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ALTIELYS CASALE MAGNAGO

TAXONOMIA E SISTEMÁTICA DE BOLETACEAE

(BOLETALES) PARA O BRASIL

Dissertação submetida ao Programa de

Pós-Graduação em Biologia de Fungos,

Algas e Plantas da Universidade

Federal de Santa Catarina para a

obtenção do Grau de Mestre em

Biologia Vegetal.

Orientador: Prof. Dra. Maria Alice

Neves

FLORIANÓPOLIS

2014

ALTIELYS CASALE MAGNAGO

TAXONOMIA E SISTEMÁTICA DE BOLETACEAE

(BOLETALES) PARA O BRASIL

Esta Dissertação foi julgada adequada para obtenção do Título de

Mestre, e aprovada em sua forma final pelo Programa de Pós-Graduação

em Biologia de Fungos, Algas e Plantas.

Florianópolis, 10 de março de 2014.

________________________

Profa. Dra. Maria Alice Neves

Coordenadora do Curso

Banca Examinadora:

________________________

Profa. Dra. Maria Alice Neves (Orientadora)

Universidade Federal de Santa Catarina

________________________

Prof. Dr. Elisandro Ricardo Drechsler dos Santos


________________________

Profa. Dra. Rosa Mara Borges da Silveira

Universidade Federal do Rio Grande do Sul

________________________

Dr. Mateus Arduvino Reck


Dedico este trabalho à minha família, aos meus amigos, ao meu companheiro,

e em especial à turma MICOLAB!

Austroboletus festivus

(Singer) Wolfe

AGRADECIMENTOS

Primeiramente agradeço minha amiga e orientadora Maria Alice

Neves por todos os desafios, ensinamentos, conversas, companherismo,

amizade e paciência, e acima de tudo pela confiança.

À Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

(CAPES) pelo auxílio financeiro sob a forma de bolsa.

À Universidade Federal de Santa Catarina, ao Departamento de

Botânica e ao Programa de Pós-Graduação em Biologia de Fungos, Algas

e Plantas por todo suporte oferecido para a execussão do projeto.

Aos docentes e pesquisadores do Programa de Pós-Graduação em

Biologia de Fungos, Algas e Plantas que de várias formas contribuíram

para o meu crescimento e para o desenvolvimento da pesquisa.

Ao Laboratório Central de Microscopia Eletrônica (LCME) da

UFSC pelas análises de Microscopia Eletrônica de Varredura.

Ao Parque das Dunas (Natal, RN), Rebio Guaribas (Mamanguape,

PB), Universidade Federal da Paraíba (João Pessoa, PB), Parque Estadual

da Serra do Conduru (BA), Rebio Augusto Ruschi (Santa Teresa, ES) e

Parque Municipal da Dunas da Lagoa da Conceição (Florianópolis, SC)

pelas permissões e apoio durante as expedições de coleta.

Aos curadores e assitentes dos herbários FLOR, ICN, PACA,

INPA, JPB, HUEFS e NY pelas permissões de visitas e disponibilização

de materiais para estudo.

Agradeço aos Micolabianos pelo companherismo nas disciplinas,

no laboratório e nas coletas, e pelo compartilhamento de seus

conhecimentos nas reuniões e confraternizações.

E todos os demais que de alguma forma me auxiliaram no

desenvolvimento deste trabalho, o meu muito obrigado!

Altielys Casale Magnago

RESUMO

O conhecimento sobre os fungos boletoides nas regiões tropicais e

subtropicais do hemisfério sul ainda é bastante limitado, havendo

escassez de dados acerca da diversidade e distribuição dos mesmos. Com

o objetivo de contribuir para o conhecimento de Boletaceae foram

estudados materiais coletados em diferentes regiões do Brasil. Quatorze

táxons foram identificados em cinco gêneros (Austroboletus, Boletellus,

Chalciporus, Fistulinella e Tylopilus), sendo que sete são espécies novas:

F. alboaurantiaca (RN), F. conduruensis (BA), F. rhytidocystidiata (ES),

T. dimorphicus (AM), T. nigrostipitatus (PB), T. pygmaeus (BA) e T. versiformis (PB). Tylopilus balloui foi registrado pela primeira vez para

o Brasil. Fistulinella cinereoalba foi registrada pela primeira vez para o

Brasil. Chalciporus trinitensis var. amazonicus foi registrado pela

primeira vez para o Espírito Santo e A. festivus é o primeiro registro para

Santa Catarina. Boletellus ananas e B. cf. lepidospora foram recoletados

nas florestas brasileiras. Para todos os táxons são apresentadas fotografias

dos basidiomas, descrições macro e micromorfológicas com ilustrações e

microscopia eletrônica de varredura (MEV) dos basidiosporos. Os

resultados mostraram uma diversidade pouco conhecida de Boletaceae

nas florestas brasileiras e uma indicação de que ainda há mais novidades

para a ciência no que diz respeito a essa família. O incremento no

conhecimento dos táxons de Boletaceae e a importância ecológica da

família devido à associação com plantas hospedeiras dá subsídios

importantes para planos de conservação em áreas onde esses táxons

ocorrem.

Palavras-chave: Agaricomycetes, Basidiomycota, neotrópicos,

sistemática, taxonomia.

ABSTRACT

Knowledge about boletoid fungi in tropical and subtropical regions of the

southern hemisphere is still quite limited and few data regarding their

diversity and distribution are available. In order to contribute to the

knowledge of the diversity of Boletaceae, specimens from different

regions of Brazil were studied. A total of 14 taxa belonging to five genera

(Austroboletus, Boletellus, Chalciporus, Fistulinella and Tylopilus) have

been identified, from which seven are new species: F. alboaurantiaca

(RN), F. conduruensis (BA), F. rhytidocystidiata (ES), T. dimorphicus

(AM), T. nigrostipitatus (PB), T. pygmaeus (BA), and T. versiformis (PB). Tylopilus balloui was registered for the first time for Brasil.

Fistulinella cinereoalba was registered for the first time for Brazil.

Chalciporus trinitensis var. amazonicus was registered for the first time

for Espírito Santo, and A. festivus is a new record for Santa Catarina.

Boletellus ananas and B. cf. lepidospora were recollected in the Brazilian

forests. Photographs of the basidiomes, fully macro and microscopic

descriptions with illustrations, and Scanning Electron Microscopy (SEM)

of the basidiospores are presented for each species. The results showed

that the diversity of Boletaceae in Brazilian forests is still not very well

known and indicates that there are more new species for science to be

described. The increase in the knowledge about the Boletaceae and the

ecological importance of the family due to the association with plants

provides data to build conservation plans in areas where these taxa grow.

Key-words: Agaricomycetes, Basidiomycota, Neotropics, systematic,

taxonomy.

SUMÁRIO

1. INTRODUÇÃO ........................................................................ 01 1.1. Caracterização de Boletaceae Chevall ............................... 01

1.2. Sistemática e classificação ................................................. 01

1.3. Distribuição no mundo e no Brasil ..................................... 03

1.4. Aspectos ecológicos e econômicos .................................... 06

2. OBJETIVOS ............................................................................. 07

3. METODOLOGIA .................................................................... 07

3.1. Áreas de coleta ................................................................... 07

3.2. Análises morfológicas ........................................................ 08

3.3. Classificação taxonômica adotada ...................................... 08

4. RESULTADOS ......................................................................... 09 4.1. Capítulo I: Artigo - New taxa and distribution records of

Tylopilus (Boletaceae) from Brazil .................................... 11

4.2. Capítulo II: Artigo - New species of Fistulinella (Boletaceae)

from Atlantic Forest, and first record of Fistulinella

cinereoalba from Brazil .................................................... 41

4.3. Capítulo III: Nota científica - New record of Austroboletus

festivus (Boletaceae) from Santa Catarina, Brazil .............. 67

4.4. Capítulo IV: Notas taxonômicas em Boletellus, Chalciporus e

Fistulinella ......................................................................... 71

5. CONSIDERAÇÕES FINAIS ................................................... 82

6. REFERÊNCIAS BIBLIOGRÁFICAS ................................... 85

1

1. INTRODUÇÃO

1.1 Caracterização de Boletaceae Chevall.

Os fungos pertencentes a Boletaceae (Chevallier 1826, Boletales sensu

Jülich 1981, Agaricales, Subordem Boletineae sensu Singer 1986, Alexopoulos

et al. 1996 e Binder & Hibbett 2006) apresentam basidiomas epígeos, conspícuos,

com desenvolvimento geralmente gimnocárpico ou pseudoangiocárpico,

terrestres, de hábito solitário ou gregário. Geralmente são robustos, com estipe

central a levemente excêntrico. A coloração do píleo e do estipe podem variar

desde tons pálidos como branco, creme, marron e rosado até cores mais vibrantes

como vermelho e alaranjado. A superfície do píleo pode ser glabra, tomentosa ou

escamosa, víscida ou seca. Apresentam himenóforo tubular, às vezes lamelar

(Phylloporus Quél., Phylloboletellus Singer), com inserção decurrente, adnata,

adnexa ou depressa. Algumas espécies apresentam reação azulada no contexto ou

na superfície do basidioma quando expostos, em resposta à oxidação de derivados

do ácido pulvínico, como o variegático, xerocômico e o atrotomentínico (Nelsen

2010). A esporada pode ser olivácea, amarelada, amarronzada, avermelhada ou

rósea. Os esporos são subglobosos, oblongos, elípticos, alongados ou fusiformes,

geralmente pigmentados e lisos, mas podendo apresentar ornamentações em

alguns gêneros (p.ex. Afroboletus Pegler & T.W.K. Young, Austroboletus

(Corner) Wolfe, Boletellus Murrill, Heimioporus E. Horak, Strobilomyces Berk.).

Os basídios são do tipo holobasídio, geralmente clavados, apresentando no

máximo quatro esterigmas. Trama do tubo bilateral ou divergente e fíbulas

presentes ou ausentes.

1.2 Sistemática e classificação

Fries (1821) em Systema Mycologicum foi o primeiro a propor um sistema

de classificação de fungos. Nesse trabalho ele sugere a criação de dois gêneros de

fungos pileado-estipitados com himenóforo tubular: Boletus L. e Fistulina Bull.,

onde no primeiro os tubos estariam conectados entre si pelo dissepimento e no

segundo os tubos estariam livres entre si.

Em 1826 Chevallier propõe Boletaceae (Agaricales) a fim de separar

basidiomas com himenóforo tubular de Agaricaceae, que apresentava himenóforo

lamelar, subdividindo Boletaceae em cinco gêneros: Boletus L., Cladoporus

(Pers.) Chevall., Fistulina Bull., Physisporus Chevall. e Polyporus P. Micheli.

Smith & Thiers (1971) reconhecem Boletaceae Chevallier (Agaricales)

circunscrevendo táxons de basidiomas carnosos, himenóforo tubular e trama do

tubo bilateral, e incluem dez gêneros (Boletus L., Boletellus Murrill,

Fuscoboletinus Pomerl. & A.H. Sm., Gastroboletus Lohwag, Gyroporus Quél.,

Leccinum Gray, Pulveroboletus Murrill, Suillus Gray, Strobilomyces Berk. e

Tylopilus P. Karst.). Phylloporus Quél., gênero com himenóforo lamelar e trama

bilateral, foi incluído em Paxillaceae, junto com Gyrodon Opat..

2

Singer (1986), mantendo a classificação com base nas características

morfológicas, subdivide Boletineae (Agaricales) em três famílias: Boletaceae

(com himenóforo tubular), Gomphidiaceae (com himenóforo lamelar e esporada

branca, creme ou marrom) e Paxillaceae (com himenóforo lamelar e esporada

acinzentada, preta ou verde oliva). Boletaceae passa a ser subdividida em seis

subfamílias: Boletoideae (Austroboletus (Corner) Wolfe, Boletus L., Boletellus

Murrill, Boletochaete Singer, Chalciporus Bataille, Fistulinella Henn.,

Leccinium Gray, Phylloboletellus Singer, Porphyrellus E.-J. Gilbert,

Pulveroboletus Murril, Tylopilus P. Karst., Veloporphyrellus L.D. Gómez &

Singer e Xanthoconium Singer), Gyrodontoideae (Gyrodon Opat., Meiorganum

Heim, Paragyrodon Singer (Singer) e Phlebopus (R. Heim) Singer),

Gyroporoideae (Gyroporus Quél.), Suilloideae (Boletinus Kalchbr.,

Psiloboletinus Singer e Suillus Gray), Strobilomycetoideae (Strobilomyces Berk.)

e Xerocomoideae (Phylloporus Quél., Tubosaeta Horak e Xerocomus Quél.).

Em Agaricales in Modern Taxonomy (Singer 1986), é reconhecido 25

gêneros e 415 espécies em Boletaceae. De acordo com o Dictionary of the Fungi

(Kirk et al. 2008) são reconhecidos 35 gêneros em Boletaceae, acomodando 787

espécies. Com a publicação de novos trabalhos, mais nove gêneros propostos

foram adicionados: Bothia (Halling et al. 2007); Durianella (Desjardin et al.

2008), Spongiforma (Desjardin et al. 2009); Heliogaster (Orihara et al. 2010);

Zangia (Li et al. 2011); Corneroboletus (Zeng et al. 2012) Sutorius, Harrya e

Austrolopilus (Halling et al. 2012a, 2012b), totalizando 44 gêneros.

Dados moleculares dão suporte à monofilia de Boletineae Singer (Binder

& Bresinsky 2002, Binder & Hibbett 2006, Drehmel et al. 2008, Neves et al. 2012

e Nuhn et al. 2013). No entanto houve uma ampliação na delimitação

morfológica, pois se incluiu em Boletales fungos com morfologias diversas como

os ressupinados e crostosos (Coniophorineae e Tapinelineae), fungos gasteroides

(Sclerodermatineae) e outros agaricoides (Hygrophoropsidaceae). Entretanto, a

morfologia boletoide surge em outros clados fora de Boletineae, como é o caso

de Boletinellus, Gyroporus e Phlebopus em Sclerodermatineae, Gyrodon em

Paxillineae e Suillus em Suillineae. Da mesma forma, morfologias gasteróides e

secotioides também se misturam com os boletoides no clado Boletineae, como é

o caso de Chamonixia e Spongiforma.

Hibbett & Thorn (2001) sugerem que o caracter tubular do himenóforo,

poderia ter surgido pelo menos cinco vezes em oito linhagens ao longo da

diversificação de homobasidiomicetos, e que somente as características

morfológicas não seriam suficientes para delimitar os táxons.

Muitos dos conceitos genéricos sobre os caracteres morfológicos e

estudos filogenéticos referentes à Boletaceae são baseados em exemplares das

regiões temperadas do hemisfério norte, sendo necessária a inclusão de espécimes

tropicais e subtropicais do hemisfério sul nos estudos moleculares e filogenéticos,

a fim de uma circunscrição mais completa dos táxons. Dessa maneira, torna-se

imprescindível fazer levantamentos mais completos acerca do grupo.

3

1.3 Distribuição no mundo e no Brasil

O conhecimento sobre os fungos boletoides nas regiões tropicais e

subtropicais do hemisfério sul ainda é bastante limitado, havendo escassez de

dados acerca da diversidade e distribuição dos mesmos. Sendo a maioria dos

registros do gênero para América do Norte, Ásia, Austrália e Europa, havendo

poucos registros para África e Américas Central e do Sul (Heinemann &

Goossens-Fontana 1954, Singer & Digilio 1957, 1960, Singer et al. 1983).

Uma das estimativas mais aceitas do número de espécies de fungos no

planeta seria de 1,5 milhões de espécies, no entanto, apenas aproximadamente

100 mil espécies foram descritas, cerca de 7% (Hawksworth et al. 1995). Há

autores que sugerem que essa diversidade ainda por ser descrita estaria

concentrada nas regioes tropicais, e que em relação aos fungos boletoides, a

América do Sul apresentaria uma diversidade restrita ao continente, tendo como

excessão os boletoides introduzidos como é o caso do gênero Suillus que se

desenvolvem em plantanções de Pinus (May 1991, Watling 2001).

No Brasil os estudos com Boletaceae ainda são muito escassos em

comparação a outros países do hemisfério norte, onde o estudo com o grupo se

iniciou há décadas (Neves & Capelari 2007). Padre Johannes Rick, considerado

o Pai da Micologia Brasileira, realizou coletas de fungos boletoides na região sul

no início do século e seus dados compilados em artigo na década de 60 (Rick

1960), onde há registro de cinco táxons de Boletales (Boletus brasiliensis Rick,

Boletus subtomentosus L., Phlebopus tropicus (Rick) Heinem. & Rammeloo,

Phylloporus flavipes Rick e Phylloporus pratensis Rick). Rolf Singer foi o

primeiro a registrar a presença de fungos boletoides nas florestas baixas da

Amazônia na década de oitenta, descrevendo vários novos táxons (Singer &

Araújo 1979, Singer et al. 1983), e Oliveira (1987) e Oliveira & Souza (1996,

2002) identificaram oito táxons boletoides em fragmentos de Mata Atlântica no

estado da Paraíba (Boletellus lepidospora E.-J.Gilbert ex Heinem, Boletellus

pustulatus (Beeli) E.-J.Gilbert, Chalciporus piperatus (Bull. Ex Fr.) Bat.,

Fistulinella violaceipora (Stev.) Sing., Gyrodon proximus Sing., Phlebopus

beniensis (Sing. & Dig.) Heinem. & Rammeloo, Phlebopus harleyi Heinem. &

Rammeloo e Phlebopus portentosus (Berk. & Br) Boedijn.

Segundo a Lista de Espécies da Flora do Brasil (Neves et al. 2012), há

registro de 43 táxons de Boletaceae para o Brasil, incluindo onze gêneros

(Austroboletus, Boletellus,, Boletus, Chalciporus, Fistulinella, Phyllobolites,

Phylloporus, Pulveroboletus, Strobilomyces, Tylopilus e Xerocomus),

distribuídas nos estados da Amazônia, Paraíba, Pernambuco, Rio de Janeiro, São

Paulo e Rio Grande do Sul. De acordo com a literatura consultada e os novos

registros apresentados neste trabalho (marcados em negrito na tabela), há 54

táxons identificados pertencentes a Boletaceae em florestas brasileiras (Tab.1).

4

Tabela 1: Táxons de Boletaceae registrados para o Brasil.

TÁXONS

UF

REFERÊNCIAS

Austroboletus festivus (Singer) Wolfe

PE

PR

SC

Singer 1970,

Watling & Meijer

1997, presente

estudo

Austroboletus graciliaffinis Singer AM Singer 1989

Austroboletus olivaceus Singer AM Singer et al. 1983

Austroboletus rionegrensis (Singer & Araujo)

Sing. AM

Singer & Araújo

1979, Singer et al.

1983

Boletellus ananas (M.A.Curtis) Murrill AM Singer et al. 1983,

presente estudo

Boletellus lepidospora E.-J.Gilbert ex Heinem. PB Oliveira 1987,

presente estudo

Boletellus pustulatus (Beeli) E.-J.Gilbert PB

Oliveira 1987,

Oliveira & Sousa

2002,

Boletus calopus Pers (sin. Boletus olivaceus

Schaeff. 1977) RS

Singer 1953, Rick

1960

Boletus cinnamomeus Rick RS Singer 1953, Rick

1960

Boletus edulis Bull. RS Sobestiansky 2005

Boletus mutabilis var. austroamericanus Rick RS Rick 1960

Boletus panormitanus Inzenga RS Rick 1960

Boletus spadiceus Schaeff. RS Singer 1953

Chalciporus trinitensis var. trinitensis (Heinem.)

Singer AM

Singer et al. 1983

Chalciporus trinitensis var. amazonicus L.D.

Gómez

AM

ES

Singer et al. 1983,

Goméz 1996,

presente estudo

Chalciporus piperatus (Bull.) Bataille

PB

PE

SC

Oliveira & Sousa

2002, Watling &

Meijer 1997,

Giachini et al.

2000

Fistulinella campinaranae Singer AM Singer et al. 1983

Fistulinella alboaurantiaca BA presente estudo

5

Fistulinella cinereoalba BA presente estudo

Fistulinella condurensis BA presente estudo

Fistulinella rhytidocystidiata ES presente estudo

Fistulinella sp1 ES presente estudo

Fistulinella violaceipora (G.Stev.) Pegler &

T.W.K. Young PB

Oliveira & Souza

2002

Phyllobolites miniatus (Rick) Singer

AM

RS

Rick 1961, Singer

et al. 1983

Phylloporus flavipes Rick RS Rick 1960

Phylloporus gymnocystis Singer AM Singer 1989

Phylloporus manausensis Singer AM Singer et al. 1983

Phylloporus pratensis Rick RS Rick 1960

Phylloporus aff. rhodoxanthus Heinem. AM Singer & Digilo

1960

Phylloporus viridis (Berk.) Singer AM Singer & Digilio

1960, Pegler 1997

Pulveroboletus duckeanus Singer AM Singer et al. 1983

Pulveroboletus roseamariae Singer AM Singer et al. 1983

Strobilomyces pauper Singer AM Singer et al. 1983

Tylopilus acutesquamosus Singer AM Singer et al. 1983

Tylopilus arenarius Singer AM Singer et al. 1983

Tylopilus balloui (Peck) Singer RN presente estudo

Tylopilus dimorphicus Magnago & Neves sp. nov. AM presente estudo

Tylopilus nigrostipitatus Magnago & M.A. Neves

sp. nov.

Tylopilus potamogeton Singer AM Singer et al. 1983

Tylopilus potamogeton var. aquarius Singer AM Singer et al. 1983

Tylopilus potamogeton var. potamogeton Singer AM Singer et al. 1983

Tylopilus pygmaeus Magnago & Neves sp. nov. BA presente estudo

Tylopilus versiformis Magnago & Neves sp. nov. PB presente estudo

Xerocomus amazonicus Singer AM Singer et al. 1983

Xerocomus amazonicus Singer var. amazonicus AM Singer et al. 1983

Xerocomus amazonicus var. obscuratus Singer &

Araujo AM

Singer et al. 1983

6

Xerocomus brasiliensis (Rick) Singer

RS

SP

Singer & Digilo

1957

Xerocomus campinaranae Singer AM Singer et al. 1983

Xerocomus chapinii Singer AM Singer et al. 1983

Xerocomus coccolobae Pegler PR Watling & Meijer

1997

Xerocomus globuliger Singer AM Singer et al. 1983

Xerocomus hypoxanthus Singer

PE

RJ

Singer & Digilio

1960, Oliveira

1987

Xerocomus inundabilis Singer AM Singer et al. 1983

Xerocomus radicicola Singer & I.J.Araujo AM Singer et al. 1983

Xerocomus scrobiculatus Singer AM Singer et al. 1983

1.4 Aspectos ecológicos e econômicos

Os fungos são considerados um dos principais componentes da

biodiversidade global, desempenhando papéis determinantes nos ecossistemas.

Assim como outros fungos, os boletoides atuam diretamente na dinâmica de

várias comunidades, principalmente pelo seu papel como decompositores,

degradando grandes moléculas e as disponibilizando no ambiente, possibilitando

a ciclagem dos nutrientes (Peya et al. 2008). Além disto, podem atuar como

simbiontes, formando associações ectomicorrízicas, onde ocorre a interação entre

o micélio fúngico e as extremidades das raízes das plantas. Nessa associação a

planta passa para o fungo produtos da fotossíntese e em troca o fungo aumenta a

capacidade de absorção de nutrientes para a planta através do micélio, além de

protegê-la contra patógenos (Agerer 1987-1991, Kothamasi 2001). Através dessa

simbiose a planta hospedeira passa a ter uma maior chance de sobrevivência e

crescimento, fato que contribui para o equilíbrio das comunidades vegetais e dos

processos de reflorestamento (Read 1999).

Aproximadamente 90% dos representantes de Boletaceae formam

ectomicorrizas, representando 18% a 25% de todos os fungos ectomicorrízicos

conhecidos (Agerer 1987-1991, Hawksworth et al. 1995). Entre as famílias de

plantas conhecidas que estabelecem esse tipo de associação estão Betulaceae

Gray, Casuarinaceae R. Br., Dipterocarpaceae Blume, Ericaceae Juss. , Fabaceae

Lindl. (Caesalpinoideae, Mimosoideae), Fagaceae Dumort., Myrtaceae Juss.,

Nyctaginaceae Juss., Pinaceae Spreng. ex Rudolphi e Salicaceae Mirb.(Brundrett

2002, Henkel 2002, Haug et al. 2005, Vellinga et al. 2009).

Além do papel ecológico, várias espécies de Boletaceae são

economicamente importantes devido ao seu valor na culinária (p.ex. Boletus

edulis Bull., conhecido popularmente como porcini; espécies de Suillus Gray

7

(Suillaceae) e popularmente conhecidas como funghi secchi; entre outras

espécies como Boletellus ananas (Curt.) Murr., Boletus pallidus Frost, Harrya

chromapes (Frost) Halling, Nuhn, Osmundson & Manfr. Binder, Retinoboletus

ornatipes (Peck) Manfr. Binder & Bresinsky, Tylopilus balloui (Peck) Singer e

Tylopilus indecisus (Peck) Murrill (Smith & Thiers 1971, Henkel et al. 2004,

Taveira & Novaes 2007).

2. OBJETIVOS

O objetivo principal do presente trabalho foi ampliar o conhecimento da

diversidade de Boletaceae nas florestas brasileiras, através de uma abordagem

taxonômica e sistemática, realizando um levantamento bibliográfico, estudo de

materiais de herbários, realização de novas coletas e identificação e registro de

novas espécies.

3. METODOLOGIA

3.1 Áreas de coleta

As áreas de estudo abrangem dois biomas, Floresta Amazônica e Mata

Atlântica. As coletas foram realizadas em trilhas nas seguintes localidades (Tab.

2), em períodos de alta pluviosidade. As coletas tiveram apoio ou foram

realizadas por colegas, incluindo Ariadne N.M. Furtado, Carlos A. S. Montoya,

Diogo H.C. Rezende, Dirce L. Komura, Maria A. Neves e Elisandro R. Drechsler-

Santos.

Tabela 2: Localidades de coletas.

Localidade Cidade UF Coordenadas Bioma

Ramal do Novo

Amanhecer, Canal

do Tarumãzinho

Mamaus AM 02°50'50''S,

60°14'08''W

Floresta

Amazônica

Parque das Dunas Natal RN 05°51'S,

35°11'W

Mata

Atlântica

(restinga)

Rebio Guaribas Mamanguape PB 06°44'14"S,

35°8'55"W

Mata

Atlântica

(tabuleiro)

UFPB João Pessoa PB 07°08'18.20"S,

34°50'49.37"W

Mata

Atlântica

Parque Estadual da

Serra do Conduru

Itacaré BA 14°24'

39°04'

Mata

Atlântica

Rebio Augusto

Ruschi

Santa Teresa ES 19°54'19.60"S,

40°34'8.20"W

Mata

Atlântica

8

Parque Municipal

das Dunas da Lagoa

da Conceição

Florianópolis S

C

27°36'46.22"S,

48°27'10.45"W

Mata

Atlântica

(restinga)

3.2 Análises morfológicas

Os basidiomas foram fotografados no local de coleta ainda frescos.

Quando possível foram realizados testes químicos com Hidróxido de Potássio

(KOH3%) e Hidróxido de Amônio (NH4OH) na superfície e no contexto do

basidioma fresco preferencialmente (Singer 1986).

Para as descrições macroscópicas seguiu-se a metodologia e

nomenclatura de Largent (1986). Os códigos de cores (ex. OAC 566), seguiu a

Tabela de cores Online Auction Color Chart (Kramer 2004). Após, os materiais

foram desidratados em uma secadora de frutas (Total Chef TCFD-05 Deluxe)

durante um período de aproximadamente 24 horas ou até a completa desidratação

dos basidiomas. Geralmente devido aos basidiomas serem robustos é necessário

seccionar os espécimes em fatias para melhor desidratação.

Após desidratados no Laboratório de Micologia (MICOLAB-UFSC),

foram realizadas as descrições microscópicas em Microscópio Óptico (Olympus

CX21), seguindo a metodologia e nomemclatura de Largent et al. (1977),

realizando lâmilas semipermanetes em água, KOH, Vermelho Congo ou

Reagente de Melzer, onde um total de 20 elementos foram medidos de cada

estrutura, como esporos, basídios, cistídios, hifas da trama, pileipelis e estipipelis.

Qm se refere a média do Quociente da medida comprimento/largura dos esporos.

As análises de Microscopia Eletrônica de Varredura (MEV) foram

realizadas no Laboratório Central de Microscopia Eletrônica da UFSC (LCME-

UFSC), onde foi retirado fragmentos do himenóforo e montados sobre uma fita

adesiva de carbono em stubs de alumínio e banhados por uma camada de 30 nm

de ouro, e observados em Micorscópio Eletrônico de Varredura a 10KeV.

Os desenhos foram realizados a mão livre a partir de imagens digitais dos

materiais em estudo.

Os exemplares foram depositados nos Herbários FLOR (Universidade

Federal de Santa Catarina, SC), HUEFS (Universidade Estadual de Feira de

Santana, BA) e no INPA (Instituto Nacional de Pesquisas da Amazônia).

3.3 Classificação taxonômica adotada

Neste trabalho foram considerados os fungos boletoides (que apresentam

píleo, estipe e himenóforo tubular), incluídos em Boletaceae de acordo com

Ainsworth & Bisby´s Dictionay of Fungi 10th edition (Kirk et al. 2008). Onde

Boletaceae compreende 35 gêneros, sendo 21 boletoides (Afroboletus Pegler &

T.W.K. Young, Aureoboletus Pouzar, Austroboletus (Corner) Wolfe, Boletus

Dill. ex Fr., Boletellus Murr., Boletochaete Sing., Bothia Halling, T.J. Baroni &

Manfr. Binder, Chalciporus Bat., Fistulinella Henn., Heimioporus E. Horak,

Leccinum S.F. Gray, Leccinellum Bresinsky & Manfr. Binder Phyllobolites

9

Singer, Porphyrellus Gilbert, Pulveroboletus Murr., Strobilomyces Berk.,

Tubosaeta E. Horak, Tylopilus Karst., Veloporphyrellus Gomez & Sing.,

Xanthoconium Sing., Xerocomus Quel.) e os demais gasteróides e agaricóides.

4. RESULTADOS

Foram identificados 30 espécimes referentes a 14 táxons, distribuídos em

cinco gêneros (Austroboletus (Corner) Wolfe, Boletellus Murrill, Chalciporus

Bataille, Fistulinella Henn. e Tylopilus P. Karst.). Abaixo (Tab. 3) a lista dos

táxons, com os números de coletores, o Estado (UF) e a formação vegetacional

do local de coleta.

Tabela 3: Táxons identificados durante o período de trabalho.

Táxons N°de coletor UF Vegetação

Austroboletus

festivus

ACM564 ACM573

ACM574 ACM575

ACM 847

SC Restinga/ Dunas

Boletellus

ananas

DLK380 AM Ombrófila densa

Boletellus cf.

lepidospora

MAN481 MAN502 PB Ombrófila densa (área

de Tabuleiro)

Chalciporus

trinitensis var.

amazonicus

ACM492

ACM528 ACM529

ES Ombrófila densa

Fistulinella

alboaurantiaca

MAN185 BA Ombrófila densa

Fistulinella

cinereoalba

ACM484 BA Ombrófila densa

Fistulinella

conduruensis


Fistulinella

rhytidocystidiata

ACM526 ES Ombrófila densa

Fistulinella sp.1 ACM491 ES Ombrófila densa

Tylopilus balloui MAN215 MAN216

MAN218 MAN255

MAN256 MAN258

MAN281

RN Restinga/ Dunas

Tylopilus

dimorphicus

DLK382 AM Ombrófila densa

10

Tylopilus

nigrostipitatus

MAN389 PB Ombrófila densa

Tylopilus

pygmaeus


Tylopilus

versiformes

MAN460 ACM269

ACM296 ACM297

PB Ombrófila densa (área

de Tabuleiro)

Alguns táxons identificados foram compilados em artigos/nota científica

e divididos em capítulos e estes formatados de acordo com as normas das revistas

sugeridas:

Capítulo I: Artigo - New taxa and distribution records of Tylopilus (Boletaceae)

from Brazil (Mycotaxon – B1 Biodiversidade).

Capítulo II: Artigo - New species of Fistulinella (Boletaceae) from Atlantic

Forest, and first record of Fistulinella cinereoaba for Brazil (Nova Hedwigia –

B1 Biodiversidade).

Capítulo III: (Aceito) Nota científica - New record of Austroboletus festivus

(Boletaceae) from Santa Catarina, Brazil (Brazilian Journal of Botany DOI:

10.1007/s40415-014-0048-3 – B3 Biodiversidade).

Capítulo IV: É apresentado os táxons que não foram incluídos nos capítulos

anteriores na forma de artigos: duas espécies de Boletellus, uma de Chalciporus

e uma de Fistulinella.

11

4.1 CAPÍTULO I: Artigo

New taxa and distribution records of Tylopilus

(Boletaceae) from Brazil

Altielys Casale Magnago, Dirce Leimi Komura & Maria Alice Neves

*Artigo a ser submetido para publicação na revista Mycotaxon.

13

New taxa and distribution records of Tylopilus (Boletaceae) from Brazil

ALTIELYS C. MAGNAGO1*, DIRCE L.KOMURA

2 & MARIA A. NEVES

1

1Departamento de Botânica, CCB, Universidade Federal de Santa Catarina

Florianópolis, Santa Catarina, , 88040-900, Brazil 2 Instituto Nacional de Pesquisas da Amazônia

Manaus, Amazonas, 69080-971, Brazil

*CORRESPONDENTE TO: [email protected]

Abstract – Four species of Tylopilus are described as new from Brazil. Tylopilus

balloui is registered for the first time for Brazil. The specimens were collected in

Tropical Brazilian Forests during the rainy season. A key to the species of

Tylopilus registered from Brazil is provided. Photographs of the basidiomes,

microscopic illustrations and Scanning Electron Microscopy of the basidiospores

are presented for each species.

Key words – Agaricomycetes, Boletales, Neotropics, systematic.

Introduction

Tylopilus P. Karst (1881) is a widespread ectomycorhizal genus in

Boletaceae, known from Australia, Asia, Europe and Americas (Karsten

1881, Heinemann & Goossens-Fontana 1954, Heinemann 1964, Smith &

Thiers 1971, Wolfe 1981, Singer et al. 1983, 1991, Wolfe & Bougher 1993,

Watling & Turnbull 1994, Nagasawa 1997, Henkell 1999, Watling & Tai-

Hui 1999, Henkell 2001, Chen 2004, Takahashi 2002, 2007, Palfer 2005,

Ortiz-Santana et al. 2007, Fulgenzi et al. 2007, Kirk et al. 2008, Halling et al.

2008, Osmoundson & Halling 2010). The traditional morphological concept

of Tylopilus includes species with stipe with or without reticulum, pore

surface usually whitish colored when young becoming pinkish with age, and

spore print pink to pinkish brown, never with olivaceous hues (Smith &

Thiers 1971, Singer et al. 1983, Nuhn et al. 2013). The basidiospores are

smooth and short to elongate (Qm<3.0).

About twenty species of Tylopilus have been described for the

Neotropics including Colombia (Halling 1989), Belize (Halling et al. 2008),

Costa Rica (Singer et al. 1983, Wolfe & Bougher 1993, Amtoft et al. 2002,

Halling et al. 2008, Osmundson & Halling 2010), Guyana (Henkel 1999,

2001, Fulgenzi et al. 2007), Honduras, Mexico, Nicaragua (Singer et al.

1983), and Venezuela (Singer & Digilo 1960). For Brazil there are three

known species and two varieties described by Singer et al. (1983) from the

14

Amazon forest in igapó and campinarana areas (T. acutesquamosus Singer,

T. arenarius Singer, T. potamogeton var. aquarius Singer, T. potamogeton

var. potamogeton Singer). In this paper we describe four new species and

register the first occurrence of Tylopilus balloui (Peck) Sing. for Brazil.

Material and methods

The collections were made between 2008 and 2013 during rainy seasons. Most

collections are from the Atlantic Forest: Universidade Federal da Paraíba - PB

(7°8'18.20"S, 34°50'49.37"W), Reserva Biológica Guaribas - PB (6°44'14"S,

35°8'55"W), Parque das Dunas - RN (5°51'S, 35°11'W); and Parque Estadual da Serra

do Conduru - BA; and there is collection also from the Amazon Forest at Ramal do

Novo Amanhecer, Canal do Tarumãzinho – AM (2°50'50''S, 60°14'08''W)).

Macroscopic features were described from fresh basidioma. Color codes (e.g.

OAC 640) were based on the Online Auction Color Chart (Kramer 2004).

Macrochemical tests were performed, when possible, according to Singer (1986).

Micro morphological features were examined with an Olympus CX21 microscope and

the use of descriptive terms follows Largent et al. (1977). Fungal tissue was

rehydrated and mounted in water, potassium hydroxide 3%, Melzer's solution or

Congo Red. At least twenty micro structures were measured for each collection

examined. Qm refer to the Quocient average length/width ratio range from the

basidiospores. For scanning electron microscopy (SEM) of the basidiospores,

fragments of the hymenophore were removed from dried basidiomes, mounted

directly on aluminum stubs using carbon adhesive tabs, and coated with 30 nm of

gold, and examined with a scanning electron microscope operating at 10KeV at

Laboratório Central de Microscopia Eletrônica da Univercidade Federal de Santa

Catarina (LCME-UFSC). The fragments were examined with a scanning electron

microscope operating at 10KeV. Line drawings were traced from digital photographs.

Voucher materials were deposited at FLOR, HUEFS, or INPA according to collection

sites (Thiers, continuously updated).

Taxonomy

Tylopilus balloui (Peck) Singer [as 'ballouii'], American Midland Naturalist

37: 104 (1947).

(FIGS 1,6AB)

= Boletus balloui Peck 1912

PILEUS 25−115 mm broad, at first convex, with age becoming plano-convex

to plano-depressed, yellow orange (OAC 789), to orange (OAC 644) with red

tones (OAC 670), finely velutinous under lens, dry, margin slightly inrolled

and entire; context 5−14 mm, whitish to yellowish (OAC 815), unchanging.

TUBES 4−13 mm long, whitish to cream (OAC 816), slightly decurrent; pores

1−2 mm broad, isodiametric, whitish, staining light orange brown upon

pressure. STIPE 30−65 mm × 8−28 mm centrally to eccentrically, subequal,

15

whitish to cream yellow (OAC 814); smooth, context cream (OAC 815),

unchanging; extreme base with white mycelium.

BASIDIOSPORES 6−9 x 3−4 μm (Qm=1.91), ellipsoid to elongate, the inner side

applanate, some bean shaped, in mass light yellow, inamyloid to weakly

dextrinoid, smooth, thin walled; hilar appendage 0.5−1 μm long. BASIDIA

27−40 x 6−10 μm, clavate, thin walled, hyaline, many with granular contents;

4-sterigmate, 4−6 μm long. CYSTIDIA on edges and sides similar in size and

shape, 32−82 x 6−13 μm, fusoid, ventricose, clavate, hyaline, some

dextrinoid. HYMENOPHORAL trama boletoid in a gelatinized matrix,

mediostratum of subparallel to interwoven hyphae, 3−5 μm wide, lateral

stratum hyphae 5−8 μm wide, inamyloid. PILEIPELLIS trichodermium,

interwoven in a gelatinized matrix, hyphae 2−5 μm wide, light brown with

gold brown contents, dextrinoid, hyphae regularly septate. PILEUS TRAMA

interwoven to subparallel, partly gelatinized, light yellow, with dextrinoid

contents. STIPITIPELLIS in two layers, first layer hymeniform, with terminal

cells 4−9 μm wide, light brown in H2O; presence of caulobasidia and

caulocystidia in variables shapes, like clavate, cylindrical, fusoid, ventricose,

capitate; lower layer with narrows hyphae with gold brown contents in H2O,

2−4 μm wide, interwoven vertically arranged in gelatinized matrix. STIPE

TRAMA parallel to subparallel, hyphae 4−15 μm broad, hyaline, inamyloid,

smooth and thin wall. CLAMP CONNECTION absent. MACROCHEMICAL

REACTIONS: NH4OH on surfaces unchanging, when test was made on dry

specimens. SPORE PRINT pinkish.

HABIT, HABITAT AND DISTRIBUTION − Solitary, scattered or caespitose on

white sand soil on dunes. In Brazil known only from Rio Grande do Norte

(present study), also known to Australia, Belize, Costa Rica, Mexico, United

States of America and Thailand (Halling et al. 2008).

SPECIMENS EXAMINED − BRAZIL. RIO GRANDE DO NORTE: Natal, Parque

das Dunas. 5°51'S, 35°11'W, 29 Apr 2008, Neves, M.A. 255, 256, 258

(HUEFS); 24 Apr 2008, Neves, M.A. 215, 216, 218 (HUEFS, FLOR); 24 May

2008, Neves, M.A. 281 (HUEFS). ADDITIONAL SPECIMENS EXAMINED: AUSTRALIA. QUEENSLAND: Tylopilus balloui.

Fraser Island, road from Central Station to Eurong. 25°29’6’’S, 153°5’18’’E, 11 Feb 2009, Halling, R.E. 9053 (NY). BELIZE. CAYO DISTRICT. Tylopilus balloui. Mountain Pine Ridge:

Douglas Da Silva, British Military Swamp. 16°58’9’’N, 88°59’38’’E, 6 Oct 2003. Halling, R.E.

8526 (NY). COSTA RICA. CARTAGO. Tylopilus oradivensis. Guarco, palo Verde. +/_ 4.5 km E of km 31 of Interamerican Highway. 9°46’34’’N, 83°56’42’’W. 1 June 2001. Halling, R.E.

8087 (NY).

COMMENTARY − These collections constitute the first record of T. balloui

from Brazil. Tylopilus balloui is a distinctive bolete, easily recognized in the

field by the yellow-orange to orange-red pileus, white to cream

hymenophore, cream to pale yellow stipe and unchanging reaction with

ammonium. The short dimensions of the spores and the trichodermium

16

pileipellis are another microscopic distinguishing features. The Brazilian

specimens described here agree with the description of T. balloui from

Guiana by Henkel (1999). Halling et al. (2008) commented that the

widespread distribution of T. balloui, combined with morphological

characteristics and genetics differences, suggest that T. balloui, as currently

circumscribed, represents a species complex rather than a single species.

Tylopilus dimorphicus Magnago & M.A. Neves sp. nov. ad. int.

(FIGS 2, 6CD)

DIAGNOSIS: Pileus grayish pink to lilac, with dark fibrils throughout; tubes pink; stipe brown with apex cream, with black reticulation, stipe context

bluing on the upper two third when exposed; basidiospores dimorphics,

ellipsoid to oblong, and cylindric to bacciliform; basidia dimorphic, 1 or 4-spores; cystidia fusoid to ventricose; pileipellis trichodermium; stipitipelis

with caulocystidia ventricose-rostrate to clavate. ETIMOLOGY: from the Latin dimorphicus = with two shapes; referring to the dimorphism of the basidia and basidiospores.

TYPE: BRAZIL, AMAZONAS: Manaus, Ramal do Novo Amanhecer, Canal do Tarumãzinho. 2°50’50’’S, 60°14’08’’W, 27 Apr 2012, Komura, D.L. 382

(HOLOTYPE, INPA).

PILEUS 55 mm broad, convex to slightly sinuate, grayish pink to lilac (OAC

513), with dark almost black finely fibrils throughout the pileus, dry, margin

slightly uplifted and entire; context 3−14 mm, cream (OAC 794),

unchanging. TUBES 4−15 mm long centrally, depressed around stipe, pink

(OAC 522); tube mouths whitish to light pink (OAC 795); pores 1−2 mm

broad, unchanging. STIPE 70 × 10−12 mm, centrally, subequal, tapering

gradually upward, brown (OAC 733), apex cream (OAC 806); reticulate,

reticulum blackish, context cream, weakling bluing on the upper two third

when exposed; base with white mycelium.

BASIDIOSPORES dimorphic, the majority 9−10 x 5−6 μm (Qm=1.68), ellipsoid

to oblong, the inner side slightly applanate to slightly concave, the minority

13−19 x 5−6 μm (Q=3.09), cylindric to fusiform, both hyaline, inamyloid,

smooth, guttulate, hilar appendage 0.5−1 μm long. BASIDIA 25−33 x 10−12

μm, clavate, thin walled, hyaline, inamyloid, with granulations, 1 or 4-spores;

sterigmate, 4−6 μm long. CYSTIDIA 29−44 x 5−9 μm, fusoid to ventricose,

frequent, hyaline, inamyloid. HYMENOPHORAL TRAMA boletoid in gelatinized

matrix, mediostratum subparallel, hyphae 3−4 μm wide, lateral stratum

hyphae 5−9 μm wide, inamyloid, smooth. PILEIPELLIS trichodermium,

terminal hyphae tapering at the apex, 61−90 x 6−9 μm, light reddish brown

with dark granulations in H2O; weakly bluing in 3% KOH, losing the

granulations; dextrinoid; oleiferous hyahae present. PILEUS TRAMA

interwoven to subparallel, light yellow, with dextrinoid granular contents.

17

STIPITIPELIS in two layers, first layer with caulocystidia frequent, ventricose-

rostrate, clavate, 30−42 x 6−8 μm wide, light brown, caulobasidia present;

second layer with narrows interwoven hyphae 2−4 μm, in a gelatinized

matrix. STIPE TRAMA with parallel to subparallel hyphae, 4−17 μm broad,

hyaline, inamyloid. CLAMP CONNECTION absent. MACROCHEMICAL

REACTIONS: NH4OH on pileus and stipe strongly bluing, the test was made

on dry specimens. SPORE PRINT pinkish.

HABIT, HABITAT AND DISTRIBUTION − Solitary on soil under trees, in

tropical Amazon campinarana, known only from the type locality. ADDITIONAL SPECIMENS EXAMINED − BRAZIL. AMAZONAS: Tylopilus aculeatus

Sing., Estrada Manaus-Caracaraí, km 45, 12 Jan 1979, Singer B 11484 (INPA); Tylopilus potomogeton var. aquarius Sing. Igarapé do Tarumãzinho, 14 Dec 1978,

Singer B 11433 (HOLOTYPE, INPA).

COMMENTARY − The material examined is very close to T.

acutesquamulosus Singer, that is characterized in the field by the blackish

fibrils over the grayish pink pileus and the reticulated stipe (Singer et al.

1983). In the description of T. acutesquamulosus, Singer cites a reddish

reaction on the hymenophore and in the context of the stipe when exposed,

this reaction was not observed in the specimen we studied. Tylopilus

dimorphicus presents dimorphic basidiospores, the majority ellipsoid to

oblong measuring 9−10 x 5−6 μm (Q=1.68), and the minority cylindric to

bacciliform measuring 13−19 x 5−6 μm (Q=3.09) and basidia with 1 or 4

spores, characteristics that were not cited for T. acutesquamulosus. However

it was not possible to examine the type of T. acutesquamulous because the

collection (R.Singer B11483) was not found at INPA.

Tylopilus potamogeton var. aquarius is also described by having two

sizes of basidiospores (8)9−11.5 x (5)5.5−7.5 μm (majority) and 11−16 x 5−6

μm (minority) (Singer et al. 1983), but analyzing the typus, these

characteristics were not so evident, and the other macro and microscopic

characteristis do not match T. dimorphicus.

Tylopilus aculeatus (unpublished – INPA 82381/ R.Singer B11484)

was collected in 1979, in the Amazon forest and was studied to compare to

our specimen. However, the dried exsiccate of T. aculeatus presents the

pileus surface composed by pyramidal squarrose scales that are very

prominent in the center, becoming less evident towards the margin and do not

look like the fibrils present on the surface pileus of T. dimorphicus. Tylopilus

aculeatus also differs from T. dimorphicus on the basidiospores that are

fusiform and not dimorphic, and on the cystidia that are versiform with

strongly dextrinoid contents.

Tylopilus nigrostipitatus Magnago & M.A. Neves sp. nov. ad. int.

(FIGS 3, 6EF)

18

DIAGNOSIS: Pileus pinkish with brownish center, convex to plano depressed,

surface velvet with small cracked areas; tubes pink, depressed around stipe;

stipe dark gray to black, lighter at the apex; with a whitish pruina throughout; pleurocystidia narrowly fusoid to slightly ventricose; cheilocystidia broadly

cylindrical to fusoid, septate; pileipellis trichodermal palisade of catenulate

hyphae.

ETIMOLOGY: from the Latin nigrostipitatus = with darkened stipe; referring

to the dark almost black colored stipe.

TYPE: BRAZIL, PARAÍBA: João Pessoa, Universidade Federal da Paraíba,

Mata da Biblioteca. 7°8'18.20"S, 34°50'49.37"W. 12 Mar 2009, Neves, M.A.

389 (HOLOTYPE, FLOR).

PILEUS 17−26 mm broad, convex to plano depressed with age, pinkish (OAC

682) with brownish center (OAC 659), surface velvet with small cracked

areas near the margin, dry; margin entire. TUBES 5−7 mm long centrally,

depressed around stipe, pink (OAC 634); tube mouths pinkish (OAC 633);

pores 1−2 mm broad, unchanging. STIPE 28−35 × 6−9 mm, centrally, tapering

gradually upward, surface dark gray to black (OAC 901), lighter at the apex;

with a whitish pruina throughout easily removed when brushed; context

whitish to cream.

BASIDIOSPORES 8–10 x 4–5 μm (Qm=1.95), ellipsoid to oblong, hyaline,

inamyloid, thick walled. BASIDIA 24–32 x 8–10 μm, clavate, thin walled,

hyaline, inamyloid; 4-sterigmate, 3–6 μm long. PLEUROCYSTIDIA 68–85 x 9–

13 μm, narrowly fusoid to slightly ventricose, hyaline, thin walled, scattered.

CHEILOCYSTIDIA 49−66 x 8−11 μm, broadly cylindrical to fusoid, septate

(1−2), hyaline. HYMENOPHORAL TRAMA parallel to subparallel, hyphae 4–9

μm wide, hyaline to light yellow, inamyloid, thin walled. PILEIPELLIS a

trichodermal palisade of catenulate hyphae, terminal cells tapering to the apex

or clavate, 12–19 x 8–10 μm, light brown, inamyloid. PILEUS TRAMA

interwoven, hyphae 5–12 μm wide, light yellow. STIPITIPELLIS repent, with

clusters of projecting cylindrical to subclavate hyphae, brownish; terminal

cells 4–7 μm wide, caulobasidia present. STIPE TRAMA parallel to subparallel,

hyphae 3-10 μm wide, light brown, inamyloid. CLAMP CONNECTIONS absent.

MACROCHEMICAL REACTIONS − NH4OH on surfaces unchanging, when test

was made on dry specimens. SPORE PRINT pinkish.

HABIT, HABITAT AND DISTRIBUTION − Growing on soil under trees, in

Atlantic forest, known only from the type locality.

COMMENTARY − Tylopilus nigrostipitatus is characterized in the field by the

pinkish pileus with brown tones, the pink hymenophore, pores 1–2 mm broad,

and dark gray to black stipe with a whitish pruina. Microscopically is

distinguished by the broadly septate cheilocystidia, narrowly fusoid and

19

scattered pleurocystidia, and pileipellis formed by a trichodermal palisade of

catenulate hyphae.

This species is very similar to T. vinosobrunneus Hongo (Chen et al.

2004), but macroscopically they differ in the overall color of the basidomes

and in the hymenophore. The pileus of T. vinosobrunneus is purple-brown to

vinaceous-brown when young, orange-brown to black when old; the tubes are

wood-brown or darker; and the stipe surface is vinaceous-brown to purple-

brown, with a reticulated apex. The pores of T. vinosobrunneus are smaller

(2–3 per mm) when compared to the pores in T. nigrostipitatus (1–2 per mm).

Microscopically T. nigrostipitatus resembles T. neofelleus Hongo, however

the later has broader ventricose pleurocystidia, larger basidiospores (11–14 ×

4–5 μm), and shorter ventricose cheilocystidia without septa and with an

obtuse apex (Chen et al. 2004).

Tylopilus pygmaeus Magnago & M.A. Neves sp. nov. ad. int.

(FIGS 4, 7AB) DIAGNOSIS: Pileus parabolic to plano-convex with age, brown to tannish

brown, velutinous, becoming dark brown when bruised; tubes withish,

adnate, slightly depressed around stipe, staining light brown under pressure; basidiospores ellipsoid; cystidia ventricose-rostrate to versiform, the majority

with golden brown contents, strongly dextrinoid; pileipellis trichodermium

which many terminal hyphae differentiated like cystidia, with golden brown contents, dextrinoid.

ETIMOLOGY: from the Latin pygmaeus = small, short; referring to the small

size of the basidiomes.

TYPE: BRAZIL, BAHIA: Itacaré, Parque Estadual da Serra do Conduru, 30

Nov 2012, Col. DHC Rezende & CAS Montoya, Magnago, A.C. 486 (HOLOTYPE FLOR).

PILEUS 11−26 mm broad, at first parabolic, becoming plano-convex with age,

brown (OAC 638) to tannish brown (OAC 721), velutinous, dry, becoming

dark brown when bruised, margin slightly inrolled and entire when young;

context 3−7 mm, cream (OAC 683). TUBES 3−6 mm long, adnate, slightly

depressed around stipe, whitish; pores 3−4 per mm, angular, staining light

brown under pressure. STIPE 22−35 × 4−8 mm, centrally, sub-equal, glabrous

to velvet, cream to light pinkish brown; context cream (OAC 683); extreme

base with white mycelium.

BASIDIOSPORES 7−9 x 4−5 μm (Qm=1.69), ellipsoid, the inner side applanate,

hyaline, inamyloid, smooth, thin walled, hilar appendage 0.5−1 μm long.

BASIDIA 25−35 x 8−10 μm, clavate, thin walled, hyaline, inamyloid; 4-

sterigmate, 3−4 μm long. CYSTIDIA on edges and sides not differentiated from

each other, very frequent and not or little projecting, 24−39 x 8−11 μm,

ventricose-rostrate to versiform, the majority with golden brown contents,

20

strongly dextrinoid and some hyaline without contents. HYMENOPHORAL

TRAMA boletoid in gelatinized matrix, mediostratum of many narrow parallel

to interwoven hyphae, 3−5 μm wide, these yellow to light yellow, lateral

stratum hyphae 3−11 μm wide, hyaline, strongly divergent. PILEIPELLIS

trichodermium consisting of erect to sub erect terminal hyphae which many

are differentiated like cystidia, with golden brown contents, dextrinoid,

terminal hyphae 28−73 x 8−10 μm. Pileus trama interwoven; hyphae 4−6 μm

wide, light yellow, some with granular dextrinoid contents. STIPITIPELLIS

hymeniform, terminal hyphae 23−42 x 7−11 μm, versiform, clavate,

ventricose, golden brown, strongly dextrinoid; caulobasidia present. STIPE

TRAMA subparallel to interwoven hyphae, vertically arranged, hyphae 3−10

μm wide, light yellow. CLAMP CONNECTIONS absent. MACROCHEMICAL

REACTIONS: NH4OH on surfaces unchanging, when test was made on dry

specimens.. SPORE PRINT pinkish.

HABIT, HABITAT AND DISTRIBUTION − Several basidiomes on soil under

trees, in Atlantic forest, known only from the type locality. ADDITIONAL SPECIMENS EXAMINED − BRAZIL. AMAZONAS: Tylopilus arenarius Sing. Estrada Manaus-Caracaraí, km 45, 3 Feb 1978, Singer B10590 (HOLOTYPE, INPA);

Tylopilus potomogeton Sing. Rio Negro, 20 km ca. de São Gabriel da Cachoeira, 20 Jan

1978, Araujo, I. 938 (PARATYPE, INPA); Tylopilus potomogeton var. aquarius Sing. Igarapé do Tarumãzinho, 14 Dec 1978, Singer B 11433 (HOLOTYPE, INPA).

COMMENTARY: Both T. pygmaeus and T. potamogeton var. potamogenton

Singer have small basidiomes, velutinous brownish pileus that are up to 36

mm broad, whitish hymenophore and stipe cream pinkisk with brown tones

(Singer et al. 1983). Microscopically, however T. potamogeton var.

potamogeton has longer basidiospores (9−12 x 6−8 μm), fusoid and often

mucronate hyaline cystidia, and trichodermal pileipellis.

Tylopilus pygmaeus is also similar to T. potamogeton var. aquarius

Singer by the arrangement and appearance of the cystidia, the pileipellis and

the stipitipellis (Singer et al. 1983). However the two sizes of the

basidiospores described in Tylopilus potamogeton var. aquarius were not

observed in T. pygmaeus. Macroscopically T. pygmaeus has smaller pores on

the hymenophore that react brown when bruised. The browning of the

hymenophore is also reported in T. potamogeton var. irengensis Henkel from

Guyana (Henkel 1999), but its morphology is very different from T.

pygmaeus.

Tylopilus versiformis Magnago & M.A. Neves sp. nov. ad. int.

FIG. 5, 7CD DIAGNOSIS: On sandy soil; pileus convex to plano-depressed, brown to tannish brown, velutinous,; tubes adnate to slightly depressed, cream to

pinkish, staining light orange-tan when bruised; stipe cream pinkish, finely light brown reticulation; basidiospores ellipsoid to phaseoliform;

pleurocystidia diverticulate to versiform, with strongly dextrinoid contents;

21

cheilocystidia subclavate to cylindrical with variable endings; pileipellis

trichodermium, golden brown, with dextrinoid granular contents.

ETIMOLOGY: from the Latin versiformis = of different shapes; referring to the

pleurocystidia with variable shapes and cheilocystidia with various endings.

TYPE: BRAZIL, PARAÍBA: Mamanguape, Reserva Biológica Guaribas,

SEMA II. 6°44'14"S, 35°8'55"W, 18 July 2009, Neves, M.A. 460 (FLOR); 15

May 2011, Magnago, A.C. 269 (ISOTYOPE FLOR); 27 May 2011, Magnago, A.C. 296 (HOLOTYPE FLOR), 297 (ISOTYPE FLOR).

PILEUS 60−92 mm broad, at first convex, with age plano-convex to plane or

plano-depressed, brown (OAC 640) to tannish brown (OAC 722), velutinous,

dry, becoming dark brown when bruised; margin slightly inrolled and entire;

context 5−13 mm, whitish to cream (OAC 683), unchanging. TUBES 6−15

mm long, adnate to slightly depressed, cream to pinkish (OAC 676); tube

mouths cream (OAC 683); pores 1−2 per mm, angular, staining light orange-

tan when bruised. STIPE 60−90 mm × 8−16 mm, centrally, tapering gradually

upward, cream pinkish throughout (OAC 683); extreme apex lighter, finely

reticulated, reticulum light brown (OAC 668), less pronounced downwards,

context cream (OAC 683), unchanging; base slightly tomentose, extreme

base with white mycelium.

BASIDIOSPORES 9−11 x 5−7 μm (Qm=1.55), ellipsoid to phaseoliform, the

inner side applanate or merely concave, faint pink, inamyloid, smooth, thin

walled, hilar appendage 0.8−1 μm long. BASIDIA 27−32 x 8−9 μm, clavate,

thin walled, hyaline, inamyloid; 4-sterigmate, 2−3 μm long. PLEUROCYSTIDIA

26−37 x 7−9 μm, frequent, diverticulate to versiform, hyaline, with internal

strongly dextrinoid contents. CHEILOCYSTIDIA 24−35 x 5−6 μm, frequent,

subclavate to cylindrical with variable endings, like spiral, hook, bifurcate

and sinuous, hyaline, inamyloid. HYMENOPHORAL TRAMA boletoid in

gelatinized matrix, mediostratum of many narrow parallel to interwoven

hyphae, 4−5 μm wide, these yellow to light yellow, lateral stratum hyphae

5−8 μm wide, hyaline, strongly divergent. PILEIPELLIS trichodermium,

golden brown, with dextrinoid granular contents; terminal hyphae 3−4 μm

wide, cylindrical, rounded ends. PILEUS TRAMA interwoven; hyphae 3−6 μm

wide, thin walled, light yellow. STIPITIPELLIS repent with clusters of

caulobasidia and golden brown caulocystidia, strongly dextrinoid. STIPE

TRAMA subparallel to interwoven hyphae, vertically arranged, hyphae 3−5

μm wide, hyaline. CLAMP CONNECTIONS absent. MACROCHEMICAL

REACTIONS: NH4OH on pileus bluing and weakly bluing on stipe, the test was

made on dry specimens. SPORE PRINT pinkish.

HABIT, HABITAT AND DISTRIBUTION − Solitary to scattered on white sandy

soil under trees, at tabuleiro area in Atlantic forest, known only from the

type locality.

22

ADDITIONAL SPECIMENS EXAMINED − BRAZIL. AMAZONAS: Tylopilus arenarius Sing.

Estrada Manaus-Caracaraí, km 45, 3 Feb 1978, Singer B10590 (HOLOTYPE, INPA);

Tylopilus potomogeton Sing. Rio Negro, 20 km ca. de São Gabriel da Cachoeira, 20 Jan 1978, Araujo, I. 938 (PARATYPE, INPA); Tylopilus potomogeton var. aquarius Sing.

Igarapé do Tarumãzinho, 14 Dec 1978, Singer B 11433 (HOLOTYPE, INPA).

COMMENTARY − Tylopilus versiformis fits better in section Potamogetones

proposed by Singer (1978) due to the combination of the bluing reaction on

the pileus and stipe with ammonia and the broadly short spores (Qm=

1.5−1.8), however shows the reticulation of the stipe, characteristic of section

Arenarii (Singer 1986). Tylopilus versiformis resembles T. potamogeton var.

irengensis from Guiana (Henkel 1999) because of the size and color of the

basidiome and the orange-tan staining of the hymenophore when bruised,

however T. versiformis has a finely light brown reticulation on the stipe,

browning on pileus surface when bruised and unchanging context when

exposed. It is also similar to T. arenarius, differing from it by the size of the

basidiospores and the morphology of the cystidia (Singer et al. 1983). The

diagnostic characteristic of T. versiformis is the diverse morphology of the

tip of the cheilocystidia.

Key to the Tylopilus known from Brazil

1. Pileus yellow orange with red tones; stipe and hymenophore whitish to

cream……………………………...……….……………………….T. balloui

1´. Pileus pinkish to brownish; stipe cream pinkish to dark gray to

black………………………………………………………………………...2

2. Pileus pink covered by finelly black fibrils; basidiospores and basidia

dimorphic………………………………………….………………..T. dimorphicus

2´. Pileus brownish, glabrous to finelly tomentose; basidiospores and basidia

monomorphic…………………………………………….………………….3

3. Stipe dark gray to black covered by a whitish

pruina………………………………………………………T. nigrostipitatus

3´. Stipe cream to pinkish, glabrous to reticulate………….…..……………4

4. Stipe reticulate…………………………………………….………….…..5

4´. Stipe glabrous to velvet…………………………………….…………....6

5. Pleurocystidia diverticulate to versiform; cheilocystidia subclavate to

cylindrical with variable endings, like spiral, hook, bifurcate and sinuous;

growing in Altantic forest restinga……………………...……..T. versiformis

5´. Cystidia fusoid to ampullaceous with narrow subobtuse to subacute neck;

growing in the Amazon campinarana………………………..…T. arenarius

6. Basidiomes short up to 35 mm tall; basidiospores 7−9 x 4−5

μm………………………………………………………….........T. pygmaeus

6´. Basidomes up to 75 mm tall; basidiospores 8-12 x 5-8

μm…………………………………………………………....T. potamogeton

23

Additional notes

Tylopilus potamogeton var. potamogeton and var. aquarius differ mainly

by the place where they grow and by characteristics of the tomentum of the

pileus. Tylopilus potamogeton var. aquarius grows mainly on lower portions

of the Amazon igapó forest where the areas remain covered by water for long

periods of the year and the tomentum is thicker and of pileus and stipe more

livid. Tylopilus potamogeton var. potamogeton grows in dryer areas and the

tomentum is thinner and the colors in part paler (Singer et al 1983).

Tylopilus acutesquamulosus was not included in this work because the

excicate was not found at INPA herbarium. Tylopilus aculeatus is an

unpublished name which specimen was deposited at INPA by Singer (INPA

82381/ R.Singer B11484).

25

FIGURE 1: Microcharacters of T. balloui (Peck) Sing. A-Basidiospores; B-Basidia; C-Cystidia;

D-Suprapileipellis; E-Stipitipellis (MAN 216). Bar (A, B, C, E) = 10 μm (D) = 25 μm.

27

FIGURE 2: Microcharacters of T. dimorphicus Magnago & M.A. Neves. A-Basidiospores; B-

Basidia; C- Basidia with 1 sterigma and basidiospore; D-Cystidia; E-Pileipellis; F-Stipitipellis (TYPE DLK 382). Bar (A, B, C, D, E, F) = 10 μm.

29

FIGURE 3: Microcharacters of T. nigrostipitatus Magnago & M.A. Neves. A-Basidiospores; B-

Basidia; C-Cheylocystidia; D-Pleurocystidia; E-Pileipellis; F-Stipitipellis (TYPE MAN 389).

Bar (A, B, C, D, E, F) = 10 μm.

31

FIGURE 4: Microcharacters of T. pygmaeus Magnago & M.A. Neves. A-Basidiospores; B-

Basidia; C-Cystidia; D-Suprapileipellis; E-Stipitipellis (TYPE, ACM 486). Bar (A, B, C, E) = 10 μm (D) = 25 μm

33

FIGURE 5: Microcharacters of T. versiformis Magnago & M.A. Neves. A-Basidiospores; B-

Basidia; C-Pleurocystidia; D-Cheilocystidia; E-Suprapileipellis; F-Stipitipellis (TYPE, ACM

296). Bar (A, B, C, D) = 10 μm (E, F) = 25 μm

35

FIGURE 6: Basidiomes in the field and Scanning Electron Microscopy (SEM) of the

basidiospores. A,B- Tylopilus balloui (Peck) Sing; C,D- Tylopilus dimorphicus Magnago & M.A. Neves; E,F- Tylopilus nigrostipitatus Magnago & M.A. Neves. (Bar A,C,E = 2.5 cm)

37

FIGURE 7: Basidiomes in the field and Scanning Electron Microscopy (SEM) of the

basidiospores. A,B- Tylopilus pygmaeus Magnago & M.A. Neves; C,D- Tylopilus versiformes Magnago & M.A. Neves. (Bar A,C= 2.5 cm)

39

Acknowledgments

Magnago AC thanks Coordenação de Aperfeiçoamento de Pessoal de Nível

Superior (CAPES) and Komura thanks Conselho Nacional de Desenvolvimento

Científico e Tecnológico (CNPq) for their fellowships. Reserva Biológica Guaribas,

Universidade Federal da Paraíba, Parque Estadual da Serra do Conduru, and Parque

das Dunas for the permits to collect and the support during fieldwork. Ariadne N.M.

Furtado helped during field collections. Thanks Carlos A.S. Montoya and Diogo H.C.

Rezende for bringing me collections from Bahia. LCME-UFSC for the MEV analyses.

INPA, HUEFS, and NY for sending material of reference for the studies. The authors

acknowledge Rafael Trevisan for reviewing the Latin names and Nathan Smith for

reviewing the English.

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from Costa Rica and Japan. Brittonia 54(4):262–265.

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from Guyana. Mycologia 99(4):622–627. Halling RE. 1989. A synopsis of Colombian boletes. Mycotaxon 34(1):93–113.

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Henkel TW. 1999. New taxa and distribution records of Tylopilus from Dicymbe forests of

Guyana. Mycologia, 91(4):655–665. Henkel TW. 2001. Tylopilus pakaraimensis, a new species of Tylopilus section Potamogetones

from Guyana. Mycotaxon 78:105–114.

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Fungi. 10th ed. CAB International University Press, Cambridge, 771pp. Kramer LA. 2004. The Online Auction Color Chart. ed. Online Auction Color Chart Company,

Stanford. 12pp. Largent DL, Johnson D, Watling R. 1977. How to Identify Mushrooms to Genus III: Microscopic

features. III. ed. Mad River Press Inc., Eureka. 148 pp.

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Boletineae. Fungal Biology, DOI: 10.1016/j.funbio.2013.04.008. Osmundson TW, Halling RE. 2010. Tylopilus oradivensis sp. nov.: a newly described member

of the Tylopilus balloui complex from Costa Rica. Mycotaxon 113: 475–483.

Ortiz-Santana B, Lodge DJ, Baroni TJ, Both EE. 2007. Boletes from Belize and the Dominican Republic. Fungal Diversity 27: 247–416.

Palfer G. 2005. Tylopilus temucensis sect. Oxydabiles (Fungi, Basidiomycota, Boletaceae), new

species and first record of the genus from Southamerican Nothofagus forest. Fungal Diversity 20:157–166.

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41

4.2 CAPÍTULO II: Artigo

New species of Fistulinella (Boletaceae) from Atlantic Forest, and

first record of Fistulinella cinereoaba for Brazil

Altielys Casale Magnago1* & Maria Alice Neves1

*Artigo a ser submetido para publicação na revista Nova Hedwigia.

43

Title: New species of Fistulinella (Boletaceae) from Atlantic Forest, and

first record of Fistulinella cinereoaba from Brazil

Altielys Casale Magnago1* & Maria Alice Neves1

1Programa de Pós-Graduação em Biologia de Fungos, Algas e Plantas,

Departamento de Botânica, CCB, Universidade Federal de Santa Catarina

Florianópolis, Santa Catarina, 88040-900, Brazil

*Author for correspondence: [email protected]

45

Abstract: Three species of Fistulinella are described as new for science.

Fistulinella cinereoalba is registered for the first time from Brazil. The specimens

were collected in the Brazilian Atlantic Forest. Fully macro and microscopic

descriptions, photographs of the basidiomes, microscopic illustrations and

Scanning Electron Microscopy of the basidiospores are presented for each

species.

Key words: Agaricomycetes, Boletales, Neotropics, systematic.

47

Introduction

The Atlantic Forest is considered one of the most important worldly hotspot

(Myers et al. 2000; Martini et al. 2007; SOS Mata Atlântica 2013), a biome with

high diversity of organisms, including many endemics species, with large

environmental variation distributed along Brazilian Atlantic coast and few inland

areas. Originally, it covered an area of 1.300.000 km2 (~ 15% of the country).

Currently, after decades of deforestation for wood extractives and agroindustry,

less than 8% of this area preserves the original biotic characteristics (Dean 1932-

1994; SOS Mata Atlântica 2013). Although boletoid species are mainly known

from several temperate environments, but a great diversity has been observed in

our studies in tropical Brazilian forests.

Fistulinella Henn. encompasses ~ 27 species, with distribution mainly

tropical (Pegler and Young 1981; Singer 1978, 1986; Singer et al. 1983, 1991;

Watling and Gregory 1989; Ortiz-Santana et al 2007; Watling 2008, Kirk et al.

2008, Fulgenzi et al. 2010). For this paper we followed the circunscription of

Fistulinella as defined by Singer (1986): a bolete species with smooth elongate-

fusoid basidiospores, some or all weakly to distinctly dextrinoid; hyaline cystidia,

without dextrinoid internal bodies; gelatinized lateral stratum in the

hymenophoral trama; hyphae without clamp connections; trichodermium,

ixotrichodermium or ixocutis pileipellis; white hymenophore that is pinkish when

mature; pink to pink-brown spore print.

There are only two records of Fistulinella from Brazil: F. campinaranae

Singer from Amazonas (Singer et al. 1983) and F. violaceipora (G. Stev.) Pegler

& T.W.K. Young from Paraíba (Oliveira & Souza 2002). In this study three new

species of Fistulinella are described, one for Espírito Santo (F. rhytidocystidiata),

and two for Bahia (F. alboaurantiaca and F. conduruensis). Fistulinella

cinereoalba Fulgenzi & T.W. Henkel is registered for the first time from Brazil.

Material and methods

Field expeditions were carried out in Espírito Santo (Southeastern Brazil) on

municipality of Santa Teresa at Reserva Biológica Augusto Ruschi

(19°54'19.60"S, 40°34'8.20"W), and in Bahia (Northeastern Brazil) on

municipality of Itacaré at Parque Estadual da Serra do Conduru and Fazenda

Marambaia (14°20’1’’S, 39°5’1’’W). The vegetation type in these areas is

Atlantic Forest and the climate is tropical humid with high annual rainfall (2800

mm), and the mean annual temperature varies between 20ºC and 31ºC. These

areas are considered hot-points within the hot-spots of the Brazilian biodiversity,

with a high level of endemism (Martini et al. 2007).

Macro and microscopic analysis of the specimens followed traditional

methods used for mushrooms (Largent 1986; Largent et al. 1977). The

48

basidiomes were slowly dehydrated at a low temperature (about 40ºC) on an

electric dryer (Total Chef TCFD-05 Deluxe). Color codes (e.g. OAC 663) for

macroscopic descriptions were based on the Online Auction Color Chart (Kramer

2004). Qm refer to the Quocient average length/width ratio range from the

basidiospores. For scanning electron microscopy (SEM) of the basidiospores,

fragments of the hymenophore were removed from dried basidiomes, mounted

directly on aluminum stubs using carbon adhesive tabs, and coated with 30 nm of

gold, and examined with a scanning electron microscope operating at 10KeV at

Laboratório Central de Microscopia Eletrônica da Univercidade Federal de Santa

Catarina (LCME-UFSC). Voucher specimens were deposited at Herbarium

FLOR at the Universidade Federal de Santa Catarina (Thiers, continuously

updated).

Taxonomy

Fistulinella alboaurantiaca Magnago & M.A. Neves sp. nov. ad. int.

Figs 1, 5AB

DIAGNOSIS: Pileus parabolic to broadly convex, yellow orange covered by a

gelatinous pellicle when young, becoming matted-fibrillose; stipe white overlain

by a gelatinous pellicle throughout; basidiospores 13−17 x 4−5 μm, subfusiform

to fusiform; pleurocystidia fusiform and cylindrical septate; cheilocystidia

cylindrical septate; pileipellis ixotrichodermal interrupted by repent hyphae.

ETIMOLOGY: Latin, albo = white, aurantiaca = orange; referring to the white stipe

and orange pileus surface.

HOLOTYPUS: Brazil. Bahia: Itacaré, Ramal de acesso à Fazenda Marambaia.

14°20’1’’S, 39°5’1’’W, elevation 100 m; 26 Aug 2006. Neves, M.A. 185

(HUEFS).

PILEUS 15–33 mm broad, parabolic to broadly convex, yellow orange (OAC 763),

covered by a gelatinous pellicle, more visible in young basidiomes, when mature

the surface become matted-fibrillose over a whitish ground, with orange brown

(OAC 786) fibrils; margin entire. TUBES 20–50 mm long, depressed around stipe,

pink-gray (OAC 676) with age; pores white in young basidiomes becoming

pinkish gray (OAC 676) in age, 1–2 per mm, isodiametric. STIPE 45–73 x 30–48

mm, centrally, subequal, surface fibrillose overlain by a gelatinous pellicle

throughout, entire white. White basal mycelium present. BASIDIOSPORES 13−17

x 4−5 μm (Qm=3.03), subfusiform to fusiform, with suprahilar depression, light

yellow, slightly dextrinoid, guttulate, smooth, thick walled. BASIDIA 27−35 x

10−12 μm, broadly clavate, thin walled, hyaline, inamyloid; 4-sterigmate, 3−4

μm long. PLEUROCYSTIDIA of two shapes: fusiform, 45−63 x 6−8 μm, hyaline,

49

inamyloid, smooth, wall slightly thick, frequent; cylindrical, 52−83 x 7−9 μm,

with one or two transverse septa occurring in upper two-third, hyaline, inamyloid,

smooth, thin walled. CHEILOCYSTIDIA 45−130 μm long, cylindrical, 4−5 μm

wide, septate, slightly interwoven in lower portion, frequent in young basidiomes.

HYMENOPHORAL TRAMA boletoid, mediostratum hyphae 4−9 μm, sub parallel,

light yellow, inamyloid, smooth and thin walled; lateral stratum divergent,

hyphae lighter imbedded in a gelatinized matrix. SUPRAPILEIPELLIS

ixotrichodermal interrupted by repent hyphae resulted by the crackled pattern of

the pileus surface, light brown, inamyloid, hyphae 5−7 μm wide.

MEDIOPILEIPELLIS with hyphae suberect to erect, 3−4 μm wide, light yellow in a

gelatinized matrix, 200−240 μm wide. SUBPILEIPELLIS repent, 40−60 μm wide,

hyphae 4−5 μm wide, subparallel to interwoven. Pileus trama with interwoven

hyphae, 4−12 μm wide, light yellow. STIPITIPELLIS with two layers, the top layer

with concentrated tufts of slightly interwoven cylindrical elements, septate, 5−8

μm wide, projecting 150−260 μm, light yellow; the lower layer 150−170 μm wide

with interwoven to sub parallel hyphae, hyphae 2−4 μm wide, immersed in a

dense gelatinized matrix. STIPE TRAMA parallel to subparallel, hyphae 5−7 μm

wide, light yellow in H2O and KOH 3%, inamyloid. CLAMP CONNECTION: absent.

SPORE PRINT: pinkish.

ADDITIONAL SPECIMENS EXAMINED: Brazil. Manaus: Fistulinella

campinaranae var. scrobiculata, Estrada Manaus, Caracaraí, km 45, 12 January

1979, Singer 11491; 25 April 1980, Singer 12131 (INPA). Guyana. Region 8

Potaro-Siparuni: Fistulinella cinereoalba, Pakaraima Mountains, Upper Potaro

River Basin, vicinity of Potaro base camp, 17 June 2002, Henkel 8471

(ISOTYPE, NY).

The diagnostic features of this species include the yellow glutinous orange pileus

surface on young basidiomes that turns matted-fibrillose on mature basidiomes;

entire white stipe; fusoid, smooth slightly dextrinoid basidiospores that are up to

17 μm long; and pleurocystidia fusiform and septate broadly cylindrical. In the

infrageneric classification of Singer (1986), F. alboaurantiaca fits in section

Fistulinella Singer due to the viscid to glutinous pileus and stipe.

Fistulinella alboaurantiaca resembles Fistulinella cinereoalba Fulgenzi

and T.W. Henkel from Guyana by the virtue of viscid basidiome, matted-

fibrillose pileus in mature basidiome, white stipe, and basidiospores that are

similar in size and shape. However F. cinereoalba has a gray pileus and

basidiospores strongly dextrinoid, pleurocystidia that are cylindrical to aciculate

and non septate, trichodermal pileipellis with evident dark yellow content weakly

dextrinoid (Fulgenzi et al. 2010).

Fistulinella campinaranae Singer is also similar to F. alboaurantiaca due

to the viscid to glutinous basidiomes with a grayish brown pileus, white stipe, and

similar basidiospores, however F. alboaurantiaca has a matted-fibrillose pileus,

cylindric pleurocystidia with one or two transverse septa, and pigmented

pileipellis (Singer et al. 1983).

50

Fistulinella cinereoalba Fulgenzi and T.W. Henkel

Figs 2, 5CD

PILEUS 16–27 mm broad, convex, finely fibrillose, initially entire grayish brown

(OAC 733) becoming matted-fibrillose over white ground with age, slightly

viscid to almost dry; margin entire; context white. TUBES 3–6 mm long centrally,

depressed around stipe, pinkish gray (OAC 753); pores gray whitish when young,

maturing to pinkish (OAC 753), 2 per mm, isodiametric. STIPE 60–71 mm high

to 2–3 mm broad at top and 3–4 mm broad at base, centrally, base fusiform,

surface whitish fibrillose with some brownish erect turfs reminding dots, overlain

by a gelatinous pellicle throughout, browning slightly with handling, context

white. BASIDIOSPORES 14–18 x 4–6 μm (Qm=3.23), subfusiform to fusiform, light

yellow, weakly dextrinoid, muliguttulate, smooth, thick walled. BASIDIA 31–37 x

10–12 μm, narrowly clavate, thin walled, hyaline, inamyloid; 4-sterigmate, 4–5

μm long. PLEUROCYSTIDIA fusiform to aciculate, 43–76 x 10–17 μm, hyaline,

inamyloid, smooth, thin walled. CHEILOCYSTIDIA of variable shapes: cylindrical,

24–42 x 3–4 μm, some cystidia with bifurcate apex; fusiform 46–52 x 7–8 μm;

and cylindrical septate, 2–4 μm wide, more frequent in young basidiome.

HYMENOPHORAL TRAMA boletoid, mediostratum of many narrow parallel hyhae,

2–4 μm broad, light yellow; lateral stratum lighter, hyphae 2–6 μm wide,

divergent. PILEIPELLIS trichodermal, with ochre content in H2O, dextrinoid,

hyphae 5–7 μm wide, round apex, regulary septate. PILEUS TRAMA interwoven,

hyphae 6–9 μm wide, light yellow. STIPITIPELLIS with two layers, up layer with

clusters of slightly interwoven cylindrical elements, septate, hyphae 4–6 μm

wide, with light yellow intracellular content in H2O; down layer with very loosely

thin hyphae, subparellel to interwoven, hyaline, immersed in a gelatinized matrix.

STIPE TRAMA composed of vertically arranged hyphae, 6–10 μm broad. CLAMP

CONNECTION: absent. SPORE PRINT: pinkish-brown.

HABIT, HABITAT AND DISTRIBUTION: Gregarious on soil under trees in

Atlantic forest. In Brazil known only from Bahia (present study), but also

registered from Costa Rica in forests dominated by Dicymbe corymbosa Spruce

ex Benth. (Fulgenzi et al. 2010).

MATERIAL EXAMINED: Brazil, Bahia: Itacaré, Parque Estadual da Serra do

Conduru, 30 Nov 2012, Col. DHC Rezende & CAS Montoya, Magnago, A.C.

484 (FLOR).

ADDITIONAL SPECIMENS EXAMINED: Guyana. Region 8 Potaro-Siparuni:

Fistulinella cinereoalba, Pakaraima Mountains, Upper Potaro River Basin,

vicinity of Potaro base camp, 17 June 2002, Henkel 8471 (ISOTYPE, NY).

Fistulinella cinereoalba is recognized macroscopically by the small to medium

stature of its basdiomes with a viscid gray pileus and white stipe, pink-gray

hymenophore. Microscopically the diagnostic characteristics are the smooth

subfusiform basidiospores, exhibiting a range of dextrinoid reactions; cylindrical

to aciculate pleurocystidia, narrow cylindrical septate cheilocystidia, and a

51

gelatinous pellicle covering the stipitipellis and pileipellis (Fulgenzi et al 2010).

This is the first record of F. cinereoalba from Brazil.

Fistulinella conduruensis Magnago & M.A. Neves sp. nov. ad. int

Figs 3, 5EF

DIAGNOSIS: Pileus ochraceous, planoconvex, slightly depressed in the center,

velutinous, dry; stipe cream, base fusiform, glabrous, slightly glutinose;

basidiospores 12−15 x 4−5 μm, fusiform; pleurocystidia lanceolate to ventricose,

frequent, and broadly cylindrical septate, scattered; cheilocystidia narrowly

cylindrical septate; pileipellis ixotrichodermal, golden brown.

ETIMOLOGY: referring to the site collection of Serra do Conduru, Bahia, Brazil.

HOLOTYPUS: Brazil. Bahia: Itacaré, Parque Estadual da Serra do Conduru. 30 Nov

2012, Col. DHC Rezende & CAS Montoya, Magnago, A.C. 485 (FLOR).

PILEUS 17–23 mm broad, planoconvex, slightly depressed in the center,

ochraceous (OAC 729) becoming lighter towards the margin, velutinous, dry;

margin entire; context white, unchanging. TUBES 1.5–3 mm long, centrally,

depressed around stipe, free, cream (OAC 816); pores 2–3 per mm, isodiametric.

STIPE 40–65 mm high to 2–3 mm broad at top and 3–5 mm broad at base,

subequal, fusiform base, glabrous, slightly glutinose, cream (OAC 857); context

white, unchanging. BASIDIOSPORES 12−15 x 4−5 μm (Qm=3.10), fusiform, light

yellow to pinkish, inamyloid to slightly dextrinoid, guttulate, smooth. BASIDIA

26−34 x 10−11 μm, clavate, thin wall, hyaline, inamyloid; 2−4 sterigmate, 3−5

μm long. Pleurocystidia in two shapes: lanceolate to ventricose, 41−78 x 6−10

μm, hyaline, inamyloid, frequent; and broadly cylindrical, 48−70 x 7−12 μm,

septate (2−3), hyaline, inamyloid, scattered. CHEILOCYSTIDIA narrowly

cylindrical, more frequent in young basidiome, 58−85 x 4−6 μm, septate, apex

rounded, breaks very easily in the septa, some of them branched.

HYMENOPHORAL TRAMA boletoid, mediostratum parallel, hyphae 3−5 μm broad,

light yellow, inamyloid; lateral stratum divergent, immersed in a gelatinized

matrix; hyphae 4−5 μm broad. SUPRAPILEIPELLIS ixotrichodermal, golden brown,

inamyloid, regularly septate, terminal cell 3−5 μm wide, apex rounded.

MEDIOPILEIPELLIS interwoven to sub erect, hyphae 2−3 μm broad, light yellow,

immersed in a gelatinized matrix. SUBPILEIPELLIS repent, hyphae 2−3 μm broad.

PILEUS TRAMA interwoven, hyphae 6−10 μm wide, light yellow. STIPITIPELLIS

with two layers, up layer with concentrated tufts of erect hyaline cylindrical

elements, septate, 5−8 μm broad, light yellow, caulobasidia present; down layer

with interwoven to subparallel hyaline hyphae, 2−4 μm wide, immersed in a

gelatinized matrix. STIPE TRAMA parallel, hyphae 3−9 μm broad, hyaline. CLAMP

CONNECTION: absent. SPORE PRINT: pinkish.

52

Fistulinella conduruensis is distinguished in the field by its ochraceous

velutinous pileus surface; pinkish hymenophore with 2–3 pores per mm, the stipe

is glabrous, slightly glutinous, and cream colored. The basidiospores are smooth,

subfusiform, with slightly dextrinoid reaction, the pleurocystidia are very

frequent and scattered, lanceolate to ventricose and septate.

Fistulinella conduruensis and Fistulinella venezuelae Singer & Digilo

(1960, as Tylopilus venezuelae) have the same overall color on the pileus and a

white stipe. However F. venezuelae have an obtuse slightly umbonate disc at the

center of the pileus, longer basidiospores (up to 21.5 μm), elongate, fusoid to

ampullaceous pleurocystidia.

Fistulinella rhytidocystidiata Magnago & M.A. Neves sp. nov. ad. int.

Figs 4, 5GH

DIAGNOSIS: Pileus chestnut brown becoming lighter with age, parabolic to

convex, velutinous to depressed fibrillose, dry; stipe pinkish covered by a white

pruina, browning with handling, slightly glutinose; basidiospores 14−22 x 4−5

μm, fusiform; pleurocystidia ventricose rostrate, winkled in the middle portion,

very frequent, and broadly cylindrical septate, scattered; cheilocystidia hyphal,

cylindrical, septate, frequent in young basidiome; pileipellis ixotrichodermal to

ixotrichodermal palisade, honey brown.

ETIMOLOGY: Latin, rhytido = wrinkled, cystidiata = cystidia, referring to the

pleurocystidia winkled in the middle portion.

HOLOTYPUS: Brazil. Espírito Santo: Santa Teresa, Reserva Biológica Augusto

Ruschi, Casa da Pedra. 19°54'19.60"S, 40°34'8.20"W, 05 Dez 2012, Magnago,

A.C. 526 (HOLOTYPE FLOR).

PILEUS 10–40 mm broad, parabolic to convex, chestnut brown (OAC 657)

becoming lighter with age (OAC 659), initially velutinous to depressed fibrillose

when mature, dry; margin entire; context white, unchanging. TUBES 4–7 mm

long centrally, strongly depressed around stipe almost free, whitish to cream

(OAC 676); pores white when young, maturing to light pink (OAC 669), 1.5–2

per mm, isodiametric. STIPE 42–80 mm high to 5–7 mm broad at top and 10–15

mm at base, subclavate fusiform, slightly glutinose, pinkish (OAC 655) covered

by a white pruina, browning with handling; context white, unchanging; extreme

base with fine white rhizomorph. BASIDIOSPORES 14−22 x 4−5 μm (Qm=3.44),

fusiform, with suprahilar depression, light yellow, inamyloid, guttulate, smooth.

BASIDIA 26−31 x 11−14 μm, broadly clavate, thin walled, hyaline, inamyloid; 4-

sterigmate, 2−3 μm long. PLEUROCYSTIDIA in two shapes: ventricose rostrate

53−71 x 9−14 μm, hyaline, inamyloid, wrinkled in the middle portion, very

frequent; and broadly cylindrical, septate (1−2) on the upper two third, 8−10 μm

wide, projecting 26−54 μm above hymenium, hyaline, inamyloid, scattered.

CHEILOCYSTIDIA hyphal, cylindrical, septate, frequent in young basidiome, 4−6

53

μm wide, projecting 86−75 μm. HYMENOPHORAL TRAMA boletoid, mediostratum

parallel, hyphae 3−5 μm wide, light yellow, inamyloid; lateral stratum divergent,

immersed in a gelatinized matrix; hyphae 4−7 μm wide. PILEIPELLIS in three

layers immersed in a gelatinized matrix. SUPRAPILEIPELLIS ixotrichodermal to

ixotrichodermal palisade, honey brown, inamyloid, regularly septate, terminal

cell 4−11 μm wide, and apex rounded. MEDIOPILEIPELLIS interwoven to sub erect,

hyphae 2−4 μm wide, pale yellow. SUBPILEIPELLIS repent, hyphae 2−3 μm wide.

PILEUS TRAMA interwoven to subparallel, hyphae 3−11 μm wide, light yellow.

STIPITIPELLIS with two layers, up layer with tufts of erect to suberect hyaline

cylindrical elements, septate, 4−10 μm wide, light yellow, caulobasidia present;

down layer with subparallel hyaline hyphae, 2−5 μm wide, immersed in a

gelatinized matrix. STIPE TRAMA parallel, hyphae 3−11 μm wide, hyaline. CLAMP

CONNECTION: absent. MACROCHEMICAL REACTIONS: NH4OH on pileus surface

becoming reddish orange, on stipe surface becoming yellow. SPORE PRINT:

pinkish brown.

ADDITIONAL SPECIMENS EXAMINED: AUSTRALIA. QUEENSLAND:

Fistulinella mollis, Landsborough. Dularcha National Park, track W of railroad

line, 8 June 2007, R.E. Halling 8985 (NY).

Fistulinella rhytidocystidiata is macroscopically recognized by the chestnut

brown finely velutinous pileus, whitish to cream hymenophore and the pinkish

stipe covered by a white pruina that turns brown when touched. Microscopically

the basidiospores are fusiform to sigmoid (14−22 x 4−5 μm); the pleurocystidia

are frequent, ventricose rostrate, wrinkled in the middle portion, but septate

cylindrical pleurocystidia are also present.

Fistulinella mollis Watling that grows widely on eucalypt forests in

Australia, is similar to F. rhytidocystidiata due to the presence of a brownish

pileus and white to pink hymenophore. However the pileus in F. mollis is viscid

to glutinous, and both the ventricose-rostrate pleurocystidia and the cylindric

pleurocystidia are absent. Fistulinella rhytidocystidiata also has similarities to the

Australian Fistulinella prunicolor (Cooke & Massee) Watling, however the latter

has a darker brown and reddish pileus that is viscid when wet, the tubes are

vinaceous pink, and the white stipe develops yellow stains with time (Watling &

Li 1999).

55

Fig 1: Microcharacters of Fistulinella alboaurantiaca (Holotype). A-

Basidiospores; B-Basidia; C-Cheilocystidia; D,E-Pleurocystidia; F-Pileipellis.

Bar (A, B, C, D, E, F) = 10 μm.

57

Fig 2: Microcharacters of Fistulinella cinereoalba (ACM 484). A-

Basidiospores; B-Basidia; C-Pleurocystidia; D-Cheilocystidia; E-Pileipellis; F-

Stipitipellis. Bar (A, B, C, D) = 10 μm (E,F) = 25 μm

59

Fig 3: Microcharacters of Fistulinella conduruensis (Holotype). A-

Basidiospores; B-Basidia; C,D-Pleurocystidia; E-Cheilocystidia; F-

Suprapileipellis; G-Stipitipellis. Bar (A, B, C, D, E) = 10 μm (F,G) = 25 μm

61

Fig 4: Microcharacters of Fistulinella rhytidocystidiata (Holotype). A-

Basidiospores; B-Basidia; C,D-Pleurocystidia; E-Cheilocystidia, F-

Suprapileipellis; G-Stipitipellis. Bar (A, B, C, D, E) = 10 μm (F,G) = 25 μm

63

Fig 5: Photographs of the basidiomes in the field, and Scanning Electron

Microscopy of the basidiospores. A,B- F. alboaurantiaca (Holotype); C,D- F.

cinereoalba (ACM 484); E,F- F. conduruensis (Holotype); G,H- F.

rhytidocystidiata (Holotype). (Bar A, C, E, G = 2.5 cm).

65

Acknowledgments

Magnago AC thanks Coordenação de Aperfeiçoamento de Pessoal de Nível

Superior (CAPES) for his fellowship. Reserva Biológica Augusto Ruschi and

Parque Estadual da Serra do Conduru for the permits to collect and the support

during fieldwork. Thanks Carlos A.S. Montoya and Diogo H.C. Rezende for

bringing me collections from Bahia. LCME-UFSC for the MEV analyses. INPA,

JPB and NY for sending material of reference for the studies. The authors

acknowledge Rafael Trevisan for reviewing the Latin names and Nathan Smith

for reviewing the English.

References

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brasileira. Tradução de Cid Knipel Moreira. I. ed. São Paulo: Companhia das

Letras, 1996. 848 pp.

FULGENZI, T.D., HALLING, R.E. & HENKEL, T.W. 2010. Fistulinella

cinereoalba sp. nov. and new distribution records for Austroboletus from Guyana.

Mycologia 102(1): 224–232.

KIRK, P.M., CANNON, P.F., MINTER, D.W. & STALPERS, J.A. 2008.

Ainsworth and Bisby’s Dictionary of the Fungi. 10th ed. CAB International

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features I. 2nd ed. Mad River Press Inc., Eureka, 166 pp.

LARGENT, D.L., JOHNSON, D. & WATLING, R. 1977. How to Identify

Mushrooms to Genus III: Microscopic features III. ed. Mad River Press Inc.,

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hot-point with a hot-spot: a high diversity site in Brazil´s Atlantic Forest.

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MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA,

G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities.

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OLIVEIRA, I.C. & SOUZA, M.A. 2002. Boletales (Hymenomycetes) no

Campus I da Universidade Federal da Paraíba, João Pessoa: III –

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ORTIZ-SANTANA, B., LODGE, D.J., BARONI, T.J. & BOOTH, E.E. 2007.

Boletes from Belize and the Dominican Republic. Fungal Diversity 27:247–416.

PEGLER, D.N. & YOUNG, T.W.K. 1981. A natural arrangement of the

Boletales, with reference to spore morphology. Transactions of the British

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SINGER, R. 1978. Note on Bolete Taxonomy II. Persoonia 9(4):421–438.

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Scientific Books, Königstein, Germany. 981 pp.

SINGER, R. & DIGILIO, L. 1960. Las boletaceas de sudamerica tropical. Lilloa

30:141–164.

SINGER, R., ARAÚJO, I. & IVORY, M.H. 1983. Ectotrophically Mycorrizal

Fungi of the Neotropical Lowlands, Especially Central Amazonia. 77. Ed.

Lubrecht & Cramer Ltd, 352 pp.

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67

4.3 CAPÍTULO III: Nota científica

New record of Austroboletus festivus (Boletaceae)

from Santa Catarina, Brazil

Altielys Casale Magnago & Maria Alice Neves

*Nota científica publicada online na revista Brazilian Journal of Botany (DOI:

10.1007/s40415-014-0048-3)

71

4.4 CAPÍTULO IV - Notas taxonômicas em Boletellus, Chalciporus e

Fistulinella.

Este capítulo inclui espécies já registradas para o Brasil que foram recoletadas e

foram redescritas incluindo fotos dos materiais frescos e de MEV dos esporos.

Boletellus ananas (M.A. Curtis) Murrill foi recoletada em região inundável da

Amazônia, onde já havia sido registrada por Singer et al. (1983). Boletellus cf.

lepidospora E.-J. Gilbert ex Heinem. foi recoletada no estado da Paraíba,no

entanto no município de Mamanguape. E Chalciporus trinitensis var. amazonicus

L. D. Goméz foi registrada pela primeira vez para o Espírito Santo, já havendo

registro desta espécie para o Amazonas. Está aqui incluída também a descrição

de uma nova espécie de Fistulinella para a ciência, ainda sem nome (Fistulinella

sp1), que não foi incluída no artigo porque o material coletado não era suficiente

e não estava em boas condições para ser designado como tipo de uma nova

espécie. Espera-se recoletar o material em boas condições e então publicar o novo

táxon futuramente.

Boletellus ananas (M.A. Curtis) Murrill, Mycologia 1(1): 10 (1909).

Fig. 1, 5ABC

=Boletus ananas M.A. Curtis 1848

Pileus 56 mm broad, convex, surface moist and scaly; fascicles of fibers forming

large depressed squarrose scales, red brown (OAC 656) to light red (OAC 615),

fading to tan or pale buff; margin slightly uplifted, apendicullate from partial veil;

context white to yellowish, readily staining blue when cut. Tubes 7−9 mm long

centrally, yellow (OAC 803), often tinged red brown, adnexa; pores 1 mm broad,

angular to elongate next to the stipe, yellow, staining blue when injured. Stipe 82

x 6 mm, subequal, surface smooth to fibrillose, whitish to pallid throughout,

reddish in the apex; context whitish to cream (OAC 815), turning red and blue

when exposed. Basidiospores 16−21 x 6−8 μm (Q=2.80), cylindrical to

subfusoid, longitudinally winged, cross-striated, faint yellow, inamyloid,

guttulate, thick walled, hilar appendage 0.5−1 μm long. Basidia 39−48 x 10−12

μm, clavate, hyaline, inamyloid, guttulate; 4-sterigmate, 2−4 μm long.

Pleurocystidia of two types: 36−60 x 9−12 μm, clavate to cylindrical, frequent

and 69−100 x 12−16 μm, ventricose-rostrate; both types hyaline and inamyloid.

Cheilocystidia similar to pleurocystidia in size and shapes. Hymenophoral trama

subparallel to parallel, hyphae 7−14 μm wide, faint yellow. Pileipellis repent to

subtrichodermal in a gelatinized matrix, golden brown, inamyloid, terminal

hyphae 5−12 μm wide. Pileus context interwoven, hyphae 4−15 μm wide, thin

walled, grayish blue in H2O, inamyloid. Stipitipellis repent, with scattered

projecting tufts of hyphae, terminal elements 6−8 μm wide. Stipe trama densely

packed of parallel hyphae, yellowish, and hyphae 3−6 μm wide, regularly septate.

Clamp connections absent. Macrochemical reactions: Imler’s reaction positive

72

in the pileus and stipe trama. The same fleeting blue reaction was also observed

in water and Congo Red. Spore print olivaceous.

Habit, habitat and distribution: Solitary on soil under trees, at

campinarana area in Amazon Forest. Registrated for Amazonas (Singer et al.

1983).

Specimens examined: BRAZIL. AMAZONAS: Manaus, Ramal Novo do

Amanhecer, Canal do Tarumãzinho. 2°50'50"S, 60°14'08" W, 27 April 2012,

Komura, D.L. 380 (INPA).

Additional specimens examined: BRAZIL. AMAZONAS: Boletellus

ananas var. minor Singer, Estrada Manaus-Caracaraí, km 125, 04 April 1978, R.

Singer, B 10913 (INPA); Boletellus fallax, Estrada Manaus-Caracaraí, km 45, 03

Aug 1978, R. Singer & I. Araújo, B 11346 (INPA).

Comentary: Boletellus ananas is distinguished by the presence of a partial

veil, that in mature basidiome hangs on the cap margin; the smooth, whitish stem

with a reddish zone near the apex; and the yellow pore surface that bruises blue

and eventually discolors reddish brown. The specimen collected was somewhat

old and moist, losing some of the diagnostic characteristics of the pileus surface,

but together with the others macro and microscopic features the specimen agreed

with the description of Boletellus ananas var. ananas (Singer et al. 1983).

Boletellus cf. lepidospora E.-J. Gilbert ex Heinem., Bull. Jard. Bot. Nat. Belg.

21: 293 (1951)

Fig. 2, 5D

Basidiospores 8−10 x 6−7 μm (Q=1.40), ellipsoid, longitudinally winged, pale

yellow, inamyloid, thick walled. Basidia 27−42 x 12−14 μm, clavate, thin walled,

hyaline, inamyloid; 4-sterigmate, 2−3 μm long. Cystidia on edges and sides not

differentiated from each, 36−56 x 7−12 μm, fusiform to ventricose, hyaline,

inamyloid. Hymenophoral trama parallel to subparallel, hyphae 4−12 μm wide,

hyaline, inamyloid, smooth and thin walled. Pileipellis trichodermal with

disarticulated terminal hyphae, acute to papilate, brownish, inamyloid, hyphae

8−15 μm wide; oileferous hyphae present. Pileus context interwoven, hyphae

6−16 μm wide, light yellow. Stipitipellis repent, with projecting tufts of

caulobasidia and caulocistidia, clavate to fusiform, 13−15 μm wide. Stipe context

parallel to subparallel, hyphae 5−12 μm wide, light yellow, inamyloid. Clamp

connections absent. Macrochemical reactions: not observed. Spore print not

observed.

Habit, habitat and distribution: Solitary on white sand soil under trees, at

tabuleiro area in Atlantic Forest. Registrated for Paraíba (Oliveira 1987).

Specimens examined: BRAZIL. PARAÍBA: Mamanguape, Reserva

Biológica Guaribas, SEMA II. 6°44'14"S, 35°8'55"W, 15 Aug 2009, Neves, M.A.

481 (FLOR); Mata da Grota, 23 Sep 2009, Neves, M.A. 502 (FLOR).

Additional specimens examined: BRAZIL. PARAÍBA: Boletellus

pustulatus (Beeli) E.-J. Gilbert, Universidade Federal da Paraíba, 02 Jul 1990,

73

I.C. Oliveira & M.F.M. Guimarães 297 (JPB); 12 Mar 1985, M.A. de Souza,

J.V.B. Silva, VL.F. Araújo & I.C. Oliveira 14 (JPB).

Commentary: Unfortunately the specimen was not described or

photographed when fresh. The lack of a good macroscopic description makes it

difficult to assert the identification of the specimen to the species level. However,

the typical elongate-fusoid spores with longitudinal ribs or striations is a typical

character to place the specimen in Boletellus. According to some macrocaracters

provided by the collector like the velvet yellow brown pileus, yellow

hymenophore, and microscopically ridged short spores with no cross-striae, the

ventricose to fusiform cystidia, and the terminal acute to papilate hyphae of the

pileipellis, this collections fits the description of Boletellus lepidospora

(Heinneman & Goossens-Fontana 1954).

Chalciporus trinitensis var. amazonicus L. D. Goméz Revta Biol. Trop.

44(Suppl. 4): 80 (1997)

Fig. 3, 5EF

Pileus 15−45 mm broad, convex to plano-convex, to plano-depressed when

mature, surface dry becoming subviscid, velvet to finely fibrillose, yellow brown

to cinnamon (OAC 683, OAC 650), with red tones; margin entire, enrolled

sometimes; context 2−4 mm, unchanging. Tubes 3−5 mm long, pinkish (OAC

655) to yellow (OAC 805), adnate; pores 1−1.5 mm broad, irregular, angular to

elongate near the margin, not staining under pressure. Stipe 21−58 mm × 3−5

mm, subequal, light brown (OAC 717) to orange red (OAC 642), smooth to finely

fibrillose; context light yellow (OAC 815), unchanging. Basidiospores 11–13 x

4–5 μm (Q=2.54), subfusiform, with suprahilar depression, pale yellow, slightly

dextrinoid in accumulation, smooth, thin walled. Basidia 25–32 x 8–10 μm,

clavate, thin walled, hyaline, inamyloid; 4-sterigmate, 3–4 μm long. Cystidia on

the edges and sides not differentiated from each other, 48–84 x 8–13 μm,

ventricose-rostrate to lanceotate, few with 1-2 septa, hyaline, inamyloid, frequent.

Hymenophoral trama divergent to subparalel in a gelatinized matrix, hyphae 7–

10 μm wide, hyaline, inamyloid, thin walled. Pileipellis repent to

subtrichodermal, reddish brown, inamyloid, terminal hyphae 5-8 μm wide. Pileus

context interwoven to subparallel, hyphae 4–12 μm wide, light yellow.

Stipitipellis repent, hyphae 4-6 μm wide, amber yellow, inamyloid. Caulocystidia

21–27 x 9–10 μm, clavate, forming scattered clusters. Stipe context parallel,

hyphae 5-13 μm wide, light yellow, inamyloid. Clamp connection absent.

Macrochemical reactions: NH4OH and KOH3% on surfaces becoming yellow to

unchanging. Spore print reddish brown.

Habit, habitat and distribution: Gregarious on soil in Atlantic Forest. First

record from Espírito Santo (present study). In Brazil also known for Amazonas

(Singer et al. 1983, Goméz 1996).

Specimens examined: BRAZIL. ESPÍRITO SANTO: Santa Teresa,

Reserva Biológica Augusto Ruschi, Casa da Pedra. 19°54' 19.60"S, 40°34'

74

8.20"W, 04 Dez 2012, Magnago, A.C. 492 (FLOR); 05 Dez 2012, Magnago, A.C.

528, 529 (FLOR).

Additional specimens examined: BRAZIL. AMAZONAS: Chalciporus

trinitensis var. amazonicus, Igarapé do Tarumãnzinho, 14 Dec 1978, R.Singer, B

11434 (INPA).

Commetary: These collections constitute the first record of Chalciporus

trinitensis var. amazonicus for the Atlantic Forest and Espírito Santo state. The

description here presented agrees with the description of Chalciporus trinitensis

by Singer et al. (1983), but differs on the size of the cystidia that are longer (48

to 84 μm) than the ones described by Singer (25–54 μm), and by the presence of

a few septate pleurocystidia that were not included in Singer's description.

The type of the species Chaciporus trinitensis was collected by

Heinemann in Trinidad in 1953 and it is characterized by having incrusted

cystidia and elongated filiform cheilocystidia (Singer et al. 1983). In Brazil

Chalciporus trinitensis was collected in Amazonas by Singer in 1978. Later on,

Goméz (1996) created the variety amazonicus for the specimen from Amazonas.

The characteristics that Goméz considered to create the variety were the presence

of shorter less incrusted cheilocystidia, basidiospores with suprahilar depression,

and the depressed hymenophore around the stipe.

Fistulinella sp. 1 Fig. 4, 5GH

Pileus 55 mm broad, convex, cinnamon (OAC 680) in the center becoming lighter

toward the margin, surface with depressed fibrils covered by a gelatinous pellicle

throughout; margin entire; context white, unchanging. Tubes 5–8 mm long

centrally, strongly depressed around stipe, almost free, pinkish gray (OAC 676);

pores whitish, 1–1.5 per mm, isodiametric. Stipe 95 mm high, 7 mm broad at top

and 15 mm broad at base, subclavate fusiform, surface glabrous, covered by a

fibrillose pinkish gelatinous pellicle, easily removable; context white,

unchanging. Basidiospores 14−16 x 4−5 μm (Q=3.19), subfusiform to fusiform,

yellow pinkish, inamyloid to weakly dextrinoid, thin walled. Basidia 21−28 x

10−13 μm, clavate, thin walled, hyaline, inamyloid, 4-spores; sterigmate 3−5 μm

long. Pleurocystidia 65−72 x 7−10 μm, fusiform, hyaline, inamyloid, scattered.

Cheilocystidia 73−80 x 10−12 μm, ventricose-rostrate, hyaline, inamyloid,

frequent. Hymenophoral trama divergent to subparalel, hyphae 4−11 μm broad,

hyaline, inamyloid, smooth and thin walled. Suprapileipellis with disarticulate

hyphae, light yellow, inamyloid, hyphae 4−6 μm wide, immersed by a gelatinous

pellicle. Mediopileipellis interwoven to suberect hyphae, in a gelatinized matrix,

hyphae 2−4 μm broad, light yellow. Subpileipellis repent, light yellow, hyphae

3−5 μm wide, subparallel to interwoven. Pileus trama interwoven, hyphae 3−14

μm broad, light yellow. Stipitipellis in two layers, uplayer repent, hyphae 2−4 μm

broad, hyaline, inamyloid; downlayer subparallel, hyphae 1−3 μm broad,

immersed in a gelatinized matrix. Stipe trama parallel, hyphae 3−5 μm wide,

hyaline, inamyloid. Clamp connection: absent. Macrochemical reactions:

75

NH4OH on pileus surface becoming orange; on stipe surface becoming light

yellow. Spore print: pinkish brown.

Habit and habitat: Growing solitary on soil in Atlantic Forest.

Specimens examined: BRAZIL. ESPÍRITO SANTO: Santa Teresa,

Reserva Biológica Augusto Ruschi, Casa da Pedra. 19°54'20.18"S,

40°34'7.02"W, 04 Dez 2012, Magnago, A.C. 491 (FLOR).

Additional specimens examined: AUSTRALIA. QUEENSLAND:

Fistulinella mollis, Landsborough. Dularcha National Park, track W of railroad

line, 8 June 2007, R.E. Halling 8985 (NY).

Commentary: Fistulinella sp.1 fits in section Fistulinella Singer due to

the viscid to glutinous pileus and stipe. More collections are needed to make a

better description because the specimen was old and some of the caracteristics

may have been lost.

There are some similarities between Fistulinella sp. 1 and Fistulinella

mollis, such as the viscid brownish pileus and the whitish stipe. However F. mollis

grows in Eucalyptus forest in Australia, and Fistulinella sp.1 has scattered

pleurocystidia fusiform and frequent pleurocystidia ventricose-rostrate; and the

pilepellis composed by disarticulate hyphae immersed in a gelatinous matrix that

are also different from the ones observed by F. mollis.

77

Figure 1: Microcharacters of Boletellus ananas (M.A. Curtis) Murrill. A-

Basidiospores; B-Basidia; C-Cystidia; D-Pileipellis; E-Stipitipellis (DLK 380).

Bar (A, B, C, D, E) = 10 μm.

79

Figure 2: Microcharacters of Boletellus cf. lepidospora E.-J. Gilbert ex Heinem.

A-Basidiospores; B-Basidia; C-Cystidia; D- Terminal hyphae from the

pileipellis; E- Stipitipellis (MAN 502). Bar (A, B, C, D, E) = 10 μm.

81

Figure 3: Microcharacters of Chalciporus trinitensis var. amazonicus L. D.

Goméz. A-Basidiospores; B-Basidia; C-Cystidia; D-Pileipellis, E-Stipitipellis

(ACM 492). Bar (A, B, C, D, E) = 10 μm.

83

Figure 4: Microcharacters of Fistulinella sp. 1. A-Basidiospores; B-Basidia; C-

Pleurocystidia; D-Cheilocystidia, E-Pileipellis (ACM 491). Bar (A, B, C, D, E)

= 10 μm.

85

Figure 5: Photographs of the basidiomes in the field, and Scanning Electron

Microscopy of the basidiospores. A,B,C- Boletellus ananas (M.A. Curtis)

Murrill; D- Boletellus cf. lepidospora E.-J. Gilbert ex Heinem.; E,F- Chalciporus

trinitensis var. amazonicus L. D. Goméz; G,H- Fistulinella sp. 1. (Bar A, C, E,

G = 2.5 cm).

87

5. CONSIDERAÇÕES FINAIS

Este trabalho amplia as pesquisas de Boletaceae para o Brasil, fornecendo

informações importantes sobre a diversidade dos táxons e sua distribuição, após

aproximadamente três décadas de ausência de novas coletas e estudos

sistemáticos sobre o grupo.

Tylopilus balloui e F. cinereoalba foram registradas pela primeira vez

para o Brasil. Austroboletus. festivus e C. trinitensis var. amazonicus foram

registrados pela primeira vez para Santa Catarina e Espírito Santo

respectivamente, e sete novas espécies foram propostas para a ciência (T.

dimorphicus, T. nigrostipitatus, T. pygmaeus, T. versiformis, F. alboaurantiaca,

F. conduruensis, F. rhytidocystidiata). Esses resultados reforçam afirmativas

recentes (Henkel 1999, 2001; Halling & Mueller 2001; Halling & Amtoft 2002;

Halling et al. 2008; Neves & Halling 2010; Neves et al. 2010) de que Boletaceae

é altamente diversa nas regiões tropicais e que propõem a mudança de paradigma

que foi aceita por anos devido à escassez de estudos e coletas em várias regiões

tropicais, incluindo o Brasil. Consequentemente, acreditamos que a partir do

incremento do número de expedições de coleta e da ampliação de áreas de coleta,

muitas novas espécies de Boletaceae ainda poderão ser propostas, além de gerar

uma ampliação na distribuição geográfica das espécies já conhecidas.

Os gêneros Tylopilus e Fistulinella apresentam certas similaridades

macroscópicas, como a coloração esbranquiçada a rósea do himenóforo e rósea

amarronzada da esporada; desta forma, as características microscópicas passam a

auxiliar nas identificações, como o tamanho e forma dos esporos. No entanto

algumas vezes não há um enquadramento perfeito na circunscrição dos gêneros,

uma vez que as espécies neotropicais são, em sua maioria, desconhecidas ou

pouco estudadas, sendo esperado que não se enquadrem exatamente nas

circunscrições propostas para as regiões temperadas.

As características moleculares, embora não abordadas nesse trabalho,

devem ser estudadas e os dados de espécimes neotropicais devem ser incluídos

nos estudos filogenéticos futuros a fim de saber como as espécies neotropicais se

encaixarão nas hipóteses filogenéticas existentes. A ampliação do estudo

filogenético incluindo dados tanto morfológicos quanto moleculares possibilitará

a geração de uma circunscrição mais completa dos táxons.

Em relação às espécies descritas por Rolf Singer em regiões da Amazônia

na década de 80 e depositados no Herbário INPA, muitas espécies apresentam

apenas o holótipo e a maioria está em estado precário de conservação. Desta

forma, torna-se necessário um estudo aprofundado dos boletáceos da região

Amazônica incluindo novas coletas nas áreas onde foram coletados os tipos para

que novas coleções de referência dos táxons amazônicos possam ser comparadas

e incorporadas ao herbário.

Uma das grandes demandas no país a respeito dos estudos com

boletáceos e de outros grupos de fungos, seria as relações ectomicorrízicas nas

florestas brasileiras nativas. Uma vez que aproximadamente 90% das espécies de

88

plantas realizam esse tipo de associação com fungos micorrízicos e tais

informações são pouco documentadas na literatura, a coleta de material e a

ampliação do conhecimento no que diz respeito aos hospedeiros é muito

importante para conhecermos melhor o equilíbrio das comunidades vegetais, o

que ajudaria também nos processos de reflorestamento e conservação dos biomas.

89

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